1. Introduction

William James framed the question of emotion-brain correspondence when he wrote, “…of two things concerning the emotions, one must be true. Either separate and special centres, affected to them alone, are their brain-seat, or else they correspond to processes occurring in the motor and sensory centres already assigned…” (1890, p. 473). In this paper, we statistically summarize the last fifteen years of neuroimaging research on emotion in an attempt to determine which of these alternatives is correct. We examine the utility of two different models of emotion that have each existed since the beginning of psychology.

2. A Locationist Account of the Brain Basis of Emotion

A locationist account of emotion assumes that the category emotion and individual categories such as anger, disgust, fear, happiness, sadness (and perhaps a few others) are respected by the body and brain (see Barrett, 2006a for a discussion). The guiding hypothesis of this natural kind model (Barrett, 2006a) or modal model (Barrett, Ochsner, & Gross, 2007) of emotion is that different emotion categories refer to states with endowed motivational characteristics that drive cognition and behavior. It is assumed that these states are biologically basic, inherited, and cannot be broken down into more basic psychological components (Izard, in press; Ekman & Cordaro, in press; Panksepp & Watt, in press). Despite these common assumptions, there is variability in how different researchers define emotions as natural kinds. Some theorists emphasize the universal characteristics of emotion categories, suggesting that each emotion category (e.g., anger) refers to a “family” of states that share a distinctive universal signal (e.g., facial behavior), physiology, antecedent events, subjective experience, and accompanying thoughts and memories (e.g., Ekman & Cordano, in press). In this view, emotions can be shaped by culture and learning, but all humans possess the capacity to experience and perceive the same core set of emotion categories. Other theorists take a developmental approach and argue that all infants are born with a set of “first order emotions” that are evolutionarily given reactions (including feelings, motivations and behaviors) to specific stimuli (e.g., Izard, in press). First order emotions form the core of the more elaborate “emotion schemas” that develop with age and learning and consist of complex combinations of emotions, cognitions, and behaviors. Still other theorists emphasize the evolutionary aspect of emotion categories, and argue that emotions are specific behavioral adaptations that are shared with other mammalian species and passed down through phylogeny (e.g., Panksepp, 1998; 2007; Panksepp & Watt, in press). Some models taking an “appraisal” approach to emotion also draw on natural kind assumptions about emotions (cf. Barrett, 2006a) by hypothesizing that dedicated cognitive mechanisms automatically make meaning of a stimulus and trigger the corresponding discrete emotion (e.g., Roseman, 1984; Scherer et al. 2003). Relatively little work from an appraisal perspective has investigated the brain basis of emotion (although see Sander et al 2003; 2007), so we do not discuss appraisal models further in this paper.

All natural kind models share the assumption that different emotion categories have their roots in distinct mechanisms in the brain and body. The mechanisms underlying discrete emotion categories have been discussed as particular gross anatomical locations (e.g., Calder, 2003, Ekman, 1999) or networks (e.g., Izard, in press; Panksepp, 1998) in the brain. These models constitute a locationist account of emotion because they hypothesize that all mental states belonging to the same emotion category (e.g., fear) are produced by activity that is consistently and specifically associated with an architecturally defined brain locale (see sections 5.1-5.4 below)¹ or anatomically defined networks of locales that are inherited and shared with other mammalian species (Panksepp, 1998; Panksepp & Watt, in press). Not all natural kind models are locationist, however; for example, some models propose that each discrete emotion is triggered by an inherited mechanism (e.g., an “affect program;” Tomkins, 1962; Ekman & Cordaro, in press) that does not necessarily correspond to a particular brain locale but rather to a specific pattern of autonomic nervous system activity. Much of the contemporary research on emotion makes locationist assumptions and in this paper we focus on the models that hypothesize single brain regions to be consistently and specifically associated with different emotion categories because they represent the most frequent hypothesis that has been tested in the cognitive neuroscience literature. We discuss specific predictions of the locationist approach in section 5, Testing Hypotheses of Brain-Emotion Correspondence (also see Figure 1).

3. A Psychological Constructionist Account of the Brain Basis of Emotion

A psychological constructionist account of emotion assumes that emotions are psychological events that emerge out of more basic psychological operations that are not specific to emotion. In this view, mental categories like anger, sadness, fear, etc. are not respected by the brain (nor are emotion, perception or cognition, for that matter; Barrett, 2009; Duncan & Barrett, 2007; Pessoa, 2008). A psychological constructionist approach to emotion is as old as the locationist approach, at least in its nascent form (e.g., Wundt, James and other early psychologists were psychological constructionists, see Gendron & Barrett, 2009). Our contemporary psychological constructionist approach shares much in common with cognitive neuroscience approaches arguing that basic psychological operations are common across diverse task domains (Cole & Schneider, 2007; Dosenbach, et al. 2006; Smith, et al. 2009; Wager et al. 2005; Wager & Smith, 2003; van Snellenberg & Wager, 2009). Like the neural context hypothesis, it assumes that the psychological function of individual brain regions is determined, in part, by the network of brain regions it is firing with (McIntosh, 2004). It is also consistent with recent evidence that largescale networks intrinsic to the brain interact to produce psychological events (Seeley et al 2007; Smith et al 2009; Spreng et al. 2010; see Deco, Jirsa & MacIntosh, 2011 for a review). In philosophy of mind, it is consistent with both a token identity and supervenience approach to mind-brain correspondence (Barrett, in press) and the mental mechanisms approach (Bechtel, 2007). We discuss the psychological constructionist view in a bit more detail because it is unfamiliar to many readers.

In our psychological constructionist model, called the “conceptual act model,” emotions emerge when people make meaning out of sensory input from the body and from the world using knowledge of prior experiences. Emotions are “situated conceptualizations” (cf. Barsalou, 2003) because the emerging meaning is tailored to the immediate environment and prepares the person to respond to sensory input in a way that is tailored to the situation (Barrett, 2006b). “Conceptual acts” could also be called “perceptual acts” because they are thought to emerge in consciousness just as visual and auditory percepts do when sensory input is automatically and effortlessly made meaningful using knowledge from prior experience. The idea is that the brain makes an initial prediction about the meaning of the sensory array in context (Bar, 2007), and the error between this initial top-down prediction and the sensory activity is quickly minimized (Friston, 2010) to produce a unified conscious field.

In psychological construction, all mental states, whether they are experienced as an instance of a discrete emotion category or not, are realized by more basic psychological operations or “ingredients” of the mind. The goal of psychology is to identify these psychological operations as “psychological primitives,” or the most basic psychological descriptions that cannot be further reduced to anything else mental (because at that point they would describe biological mechanisms). These basic psychological operations are not functionally specific to any discrete emotion category, or even to the category emotion itself. Instead, they are functionally selective for emotion on certain occasions. Because our own model is relatively new, our current model has not identified the most primitive level of psychological description, and it is not yet possible to definitively claim what the most basic psychological operations of the mind are. What we propose is a set of basic domains of psychological function that are a first approximation in the trajectory of a longer research program to identify psychological primitives; these will no doubt be refined as research proceeds in the coming years.

One operation in all psychological constructionist models of emotion is some form of sensory input from the body, such as raw somatic, visceral, vascular and motor cues (James, 1884), arousal (Duffy, 1957; Mandler, 1975; 1990; Schachter & Singer, 1962), or affect (Wundt, 1897; Harlow & Stagner, 2932; Hunt, 1941; now called core affect; Barrett 2006b; Barrett & Bliss-Moreau, 2009; Russell, 2003; Russell & Barrett, 1999). In our psychological constructionist view, we refer to this basic psychological domain as “core affect.” In psychology, the word “affect” is used to mean anything that is emotional. Core affect, on the other hand, is a term used to describe the mental representation of bodily changes that are sometimes experienced as feelings of hedonic pleasure and displeasure with some degree of arousal (Barrett & Bliss-Moreau, 2009; Russell & Barrett, 1999; Russell, 2003). Core affect is realized, in part, by visceral control systems that help organisms deal with motivationally salient stimuli in the environment. A functioning peripheral nervous system is not necessary for a person to experience a core affective state (e.g., Critchley et al. 2001) as long as they have some prior experiences to provide them with central nervous system representations of bodily states. However, in healthy individuals, core affect is usually accompanied by somatovisceral, kinesthetic, proprioceptive, and neurochemical fluctuations that take place within the core of body and are represented in the brain. Changes in core affect are a homeostatic barometer – the body’s way of representing whether objects in the environment are valuable or not in a given context. The concept of core affect shares much in common with the idea that bodily cues constitute a core ingredient in mental life (e.g., the idea that being embodied is essential to consciousness; Craig, 2009; Damasio, 1999; the idea that feelings are a common currency for valuation of objects in the world; Cabanac, 2002). We assume that core affect is not psychologically meaningful unless it is attached to an object; it is made meaningful via a second basic psychological operation, described below.

Definitions

Natural kind approach. A theoretical framework for understanding the ontology of emotions. The natural kinds approach assumes that emotion categories like anger, sadness, fear, etc. map on to biological categories that are given by the brain and body and cannot be reduced to more basic psychological parts.

Locationist approach. Many national kind models of emotion conform to a locationist approach where discrete emotion categories (e.g., anger) are assumed to be consistently and specifically localized to discrete brain locales or anatomical networks.

Psychological constructionist approach. A theoretical framework for understanding the ontology of emotions. The psychological constructionist approach assumes that emotion categories like anger, sadness, fear, etc. are common sense categories whose instances emerge from the combination of more basic psychological operations that are the common ingredients of all mental states.

Core affect. The mental representation of bodily sensations that are sometimes (but not always) experienced as feelings of hedonic pleasure and displeasure with some degree of arousal. Core affect is what allows an organism know if something in the environment has motivational salience (i.e., is good for it, bad for it, approachable or avoidable). Barring organic abnormality, core affect is accompanied by somatovisceral, kinesthetic, proprioceptive, and neurochemical fluctuations that take place within the core of body and feed back to be represented in the brain.

Conceptualization.The process by which sensations from the body or external world are made meaningful in a given context using representations of prior experience. Conceptualization occurs in a situated fashion (as in “situated conceptualization;” see Barslou et al., in press), drawing on the representations of prior experience that are activated by the present physical and psychological situation.

Executive attention. The process by which some representations are selectively enhanced and others are suppressed. This is also known as “endogenous,” “controlled,” or “goal-based” attention and can be exerted both volitionally and without the conscious experience of volition. Executive attention can shape the activity in other processes like core affect, conceptualization or language use. In the case of emotion, executive attention foregrounds certain core affective feelings and exteroceptive sensory sensations in a moment and guides which situated conceptualizations are brought to bear to make meaning of those sensations in the given context.

Emotion words. The set of words that ground the abstract categories that humans experience and communicate about. In the case of abstract categories like emotions, words are “essence placeholders” that help cohere feelings, behaviors, facial expressions, etc. together as instances of a meaningful category.

Neural reference space. The set of neurons that are probabilistically involved in realizing a class of mental events (such as anger, or even emotion).

Functional selectivity. When a set of neurons show a consistent increase in activation for one mental state (e.g., anger, disgust, emotion) or basic psychological operation (e.g., categorization, core affect) more so than for others in a given instant. The neurons are not specific to any mental state, although they might be more frequently activated in some than in others. Functional selectivity might occur because a brain region supports a more basic psychological operation that helps to construct a certain mental state (e.g., the amygdala supports detection of salient exteroceptive sensations and is functionally selective for perceptions of fear). A brain area might be functionally selective for one mental state or even one basic psychological operation in one instance and another state or operation in another instance (e.g., ventromedial prefrontal cortex helps to realize both core affect and conceptualization).

All psychological constructionist models include a second basic psychological operation by which internal sensory cues or their associated affective feelings are automatically and effortlessly made meaningful (i.e., experienced as related to or caused by an event or object, usually in the external surroundings). Candidates for this second psychological operation include ideas (Wundt, 1897), social affiliation (Schachter & Singer, 1962), attribution (Russell, 2003), or as we propose in our model, categorization as situated conceptualization (Barrett, 2006b). The process of “conceptualization” (and the other operations that support it, like executive attention) links perceptions of sensory input from the world with input from the body to create a meaningful psychological moment. In our hypothesis, people automatically make meaning of their core affective state by engaging in a situated conceptualization that links it to an object or event. Conceptualization is the process by which stored representations of prior experiences (i.e., memories, knowledge) are used to make meaning of sensations in the moment (Wilson-Mendenhall et al. in press). A person can make the situated conceptualization that core affect is a physical symptom (e.g., a racing heart), a simple feeling (e.g., feeling tired or wound up) or as an instance of a discrete emotion category (e.g., anger v. fear). And at other times, core affect is perceived as part of an object itself rather than one’s reaction to it. For instance, a food is delicious or distasteful, a painting is beautiful or garish, or a person is warm or cold. Because we hypothesize that people make meaning of their core affective states in context, experiencing them as a part of an emotion, perception, belief, or judgment, a psychological constructionist account does not simply reduce the category of emotion to positive or negative affect (as is often claimed in summaries of “dimensional models of emotion;” e.g. Fontaine et al. 2007; Keltner et al. 2003). Conceptualization can be said to produce cognitive appraisals realizing emotion (Barrett, Mesquita et al. 2007), where such appraisals are descriptions of the features or properties of emotional experience (Clore & Ortony, 2008). In many appraisal models, the assumption is that the brain contains a series of specific cognitive appraisal mechanisms (e.g., there is a specific mechanism to appraise the novelty of an object or whether one’s goals are blocked) that when configured into a particular pattern trigger discrete emotions. In our model, we do not propose any new or unique mental processes that cause emotion; instead, we propose a mechanism (categorization) that has been well documented in the psychological and cognitive neuroscience literature. Categorization (or conceptualization) is a fundamental process in the human brain that functions like a chisel, leading people to attend to certain features in a sensory array and to ignore others. Only some of the wavelengths of light striking our retinas are transformed into seen objects, only some of the changes in air pressure registered in our ears are heard as words or music, and only some bodily changes are experienced as emotion. To categorize something is to render it meaningful. It then becomes possible to make reasonable inferences about that thing, to predict what to do with it, and to communicate our experience of it to others. There are ongoing debates about how categorization works, but the fact that it works is not in question.

In our model, categorization in the form of situated conceptualization is realized in a set of brain regions that re-constitutes prior experiences for use in the present. This set of brain regions has also been called the episodic memory network (e.g., Vincent et al. 2006) or the default network (e.g., Raichle et al. 2001) and is active when people recall the past (e.g., Buckner & Carroll, 2007; Schacter et al. 2007; see McDermott et al. 2009 for a meta-analysis), imagine the future (e.g., Addis et al. 2007; see Hassabis & Maguire, 2009; Moulton & Kosslyn, 2009; Schacter et al. 2007), make context-sensitive predictions about others’ thoughts and feelings (e.g., as in theory of mind; Saxe & Kanwisher, 2003; see Mitchell, 2009), or make meaning of exteroceptive sensations (e.g., context-sensitive visual perception; Bar et al. 2006; see Bar, 2009). In emotion, we hypothesize that this psychological operation makes a prediction about what caused core affective changes within one’s own body or what caused the affective cues (e.g., facial actions, body postures, or vocal acoustics) in another person, and this prediction occurs in a context-sensitive way (with the result that core affect in context is categorized as an instance of anger, disgust, fear, etc.; Barrett, 2006b; 2009b; e.g., Barrett & Kensinger, 2010; Wilson-Mendenhall et al., in press; Lindquist & Barrett, 2008). In doing so, conceptualization draws on prior experiences and perceptions of emotion to realize the emotional gestalts that make up part of what Edelman calls “the remembered present” (cf. Edelman, 1989; see Barrett, Mesquita et al., 2007; Barrett, 2009b).

Our model proposes two additional operations that are important to the psychological construction of emotion. We hypothesize that emotion words that anchor emotion categories work hand in hand with conceptualization (Barrett, 2006b; Barrett, Lindquist, & Gendron, 2007).

Emotion words are essential to our model because we assume that the instances of any emotion category (e.g., anger) that are created from affective feelings don’t have strong statistical regularities in the real world or firm natural category boundaries (for a discussion of the empirical evidence, see Barrett, 2006a; 2009; Barrett, Lindquist et al., 2007). In our view, emotion categories are abstract folk categories that are socially constructed (Barrett, 2009a). As with all abstract categories, in the absence of strong perceptual statistical regularities within a category, humans use words as the glue that holds the category together (Barsalou & Weimer-Hastings, 2005). In fact, even infants routinely use the phonological form of words to make conceptual inferences about novel objects that share little perceptual similarity (Dewar & Xu, 2009; Ferry, Hespos & Waxman, 2010; Xu, 2002) and we believe that adults do the same thing. Since words are in part represented via situated simulations of prior experiences (e.g., Simmons et al. 2008), we expect emotion words to work together with conceptualization when perceivers make meaning of core affective states.

Executive attention is the fourth operation that is particular to our psychological constructionist approach (Barrett, 2009a; Barrett, Tugade, & Engle, 2004). Executive attention helps direct the combination of other psychological operations to produce an emotional gestalt. At any point in time, the brain is processing information from the body (core affect), information from outside the body (exteroceptive sensory information) and representations of prior experiences (conceptualizations). For instance, many different representations of the past might become active to make meaning of a core affective state. We hypothesize that executive attention helps determine which representations are utilized to make meaning of that state, and which are suppressed (c.f. Barrett, 2009b; see Barrett, Tugade, & Engle, 2004, for a discussion). Executive attention can also control which exteroceptive sensory representations are favored for additional processing, or if core affect is consciously represented in awareness. Importantly, executive attention need not be volitional or effortful and can operate well before subjective experience is generated (Barrett, Engle & Tugade, 2004). We acknowledge that additional operations are likely important to the construction of emotion and will be incorporated into our model as research accrues.

In the past, most research that found brain correlates of emotion merely assumed that their results were consistent with a locationist approach (e.g., the basic emotion approach) because these were the only models to map psychological states to a biological level of analysis in a way that was linked to evolution; constructionist hypotheses (which where typically social, rather than psychological) were restricted to the psychological level in a way divorced from evolution. But this is an accident of history. In fact, there are very clear brain hypotheses that develop from a psychological constructionist view (Barrett, 2006b), and our psychological constructionist approach is the first that attempts to map basic psychological operations to brain networks that comprise instances of a psychological category like emotion, or to the subordinate categories of anger, sadness, fear, disgust, and happiness (see also Barrett, 2006a, b, 2009a, b; Barrett, Lindquist, Bliss-Moreau, Duncan, Gendron et al. 2007; Barrett, Mesquita, Oschner & Gross, 2007; Kober, Barrett, Joseph, Bliss-Moreau, Lindquist, & Wager, 2008). Our hypothesized psychological operations, as they currently stand, are associated with assemblies of neurons within distributed networks (rather than a one to one mapping of ingredient to network). We hypothesize that these networks combine and constrain one another like ingredients in a recipe, influencing and shaping one another in real time according to the principles of constraint satisfaction (Barrett, Ochsner, & Gross, 2007). With more research, it will be possible to identify the distributed brain networks that are associated with the most basic psychological operations of the mind.

Together, the functional networks that instantiate basic psychological operations during emotion experiences and perceptions form the “neural reference space for discrete emotion.” According to Gerald Edelman (1989), a “neural reference space” is made up of the neurons that are probabilistically involved in realizing a class of mental events (such as anger, or even emotion).² The functions of distinct brain areas within the neural reference space are best understood within the context of the other brain areas to which they are connected (either anatomically or because of the timing and coordination of neural activity) and in terms of the basic psychological operations they are functionally selective for in a given instance. Unlike a locationist approach, which hypothesizes that a single brain region will be consistently and specifically activated across instances of a single emotion category, a psychological constructionist approach hypothesizes that the same brain areas will be consistently activated across the instances from a range of emotion categories (and although it is beyond the scope of this paper, even in nonemotional states), meaning that that brain region is not specific to any emotion category (or even to emotion per se). We focus on the brain regions that we believe are hubs in the networks corresponding to basic psychological operations and discuss specific predictions in section 5, Testing Hypotheses of Brain-Emotion Correspondence (also see Figure 2).

4. Meta-analysis of Neuroimaging Studies on Emotion

In this paper, we report a meta-analysis of neuroimaging studies on emotion to assess whether the data are more consistent with a locationist or psychological constructionist account of emotion. In our meta-analysis, strong evidence for a locationist account would be found if instances of an emotion category (e.g., fear) are consistently and specifically associated with increased activity in a brain region (or a set of regions within an anatomically inspired network) across published neuroimaging studies. Consistency refers to the fact that a brain region shows increased activity for every instance of an emotion category (e.g., the amygdala shows increased activity each time a person experiences an instance of the category fear). Specificity refers to the fact that a given brain region is active for instances of one (and only one) emotion category (e.g., the amygdala does not show increased activity when a person is experiencing an instance of anger, disgust, happiness or sadness). Support for a psychological constructionist view, in contrast, would be found if the same brain region(s) were involved in realizing instances of several emotion categories—and, furthermore, if the brain region(s) are more generally important to realizing a basic psychological operation (e.g., core affect, conceptualization, language, or executive attention). From this perspective, we would not expect instances of any emotion category to be specifically related to increased activation in any single brain region or set of regions. A brain region might be functionally selective for a given emotion category in a given instance, however, because it helps realize a more basic operation that contributes to the emergent state.

In 2005, we began our meta-analytic project to probe the brain basis of emotion. We have since published one chapter (Wager et al. 2008) and two papers (Kober et al. 2008; Barrett, Mesquita, et al. 2007) reporting our findings for neuroimaging studies of discrete emotion and affect published between 1990 and 2005. Supporting a psychological constructionist approach to emotion, we found that the neural reference space for emotion and affect could be inductively parsed into six distributed functional groups of brain regions (i.e., regions consistently coactivated across studies) using a series of multidimensional scaling and cluster analyses (Kober et al. 2008). These functional groups can be mapped to the hypothesized psychological operations that we derived from behavioral data (e.g., Barrett, 2006). See Figure 2.

4.1 Analysis Strategy. In the present paper, we expanded upon our initial meta-analytic efforts to directly compare the locationist vs. the psychological constructionist approach for neuroimaging studies of discrete emotion. See supplementary materials for a detailed discussion of our meta-analytic methods. In comparing these hypotheses, we are comparing a hypothesis with very specific empirical requirements (i.e., evidence for consistency and specificity in brain-emotion correspondence) to a hypothesis with more flexible empirical requirements (i.e., evidence of multiple operations across multiple categories). Given the popularity of locationist models of emotion, we made analysis choices that favored a clear and unbiased test of the locationist approach, even though it disadvantaged us in testing the full scope and power of the psychological constructionist approach. After updating our database to include papers from 2006 and 2007, we exclusively sampled studies that focused on discrete emotion experiences or perceptions to increase the likelihood that we would find consistent and specific brain localizations corresponding to these categories, should they exist. We also conducted a number of statistical analyses with the potential to yield evidence in favor of a locationist account (outlined below).

4.1.1. The neural reference space for discrete emotion. We began by estimating the neural reference space for discrete emotion. This space refers to the brain regions that show a consistent increase in activation for the experience or perception of instances of anger, sadness, fear, disgust, and happiness. A brain region might appear in this space because its activation consistently increases in studies of one discrete emotion categories but not others, some categories but not others, or all categories of emotion. Alternatively, a brain region could appear in this space even when it does not consistently have increased activation during any discrete emotion category per se, but because it has consistent increases during instances of the entire category emotion (e.g., the brain region shows consistent increases in activation in some but not all studies of anger experience, anger perception, fear experience, fear perception, etc. so that the region is consistently activated across the category emotion, but is not specific to any discrete emotion category). Our derived neural reference space for discrete emotion (Figure 3; Table S3 in supplementary materials) closely resembles that reported in Kober et al. (2008), even when limiting our analysis to studies of discrete emotion and including papers from 2006-2007. Next, we examined whether any emotion categories were more likely to be associated with increased activity in certain brain areas than others.

4.1.2. Density analyses. Within the neural reference space, we first searched over the brain for voxels with more consistent activation (within 10 mm) for instances of one emotion category than all others (e.g., for voxels that reached family-wise error-rate corrected significance in the comparison [fear perception v. perception of other categories]). This analysis yielded a series of statistical maps reflecting whether each voxel was more frequently activated in studies of each emotion category vs. the average of the others, accounting for the different numbers of studies in different categories and the base-rate of background activation across the brain for each emotion category. These analyses are standard for neuroimaging meta-analysis (see Wager et al. 2007) and are described in detail in the supplementary materials. The density analyses speak to whether increases in a brain region are consistently associated with the experience or perception of instances of an emotion category. This provides one kind of information about the consistency and specificity of brain activity for particular emotion categories by considering the activity in each region, for each emotion type, relative to background activation levels across the brain.

4.1.3. c²analyses. We next probed the voxels identified in the density analysis further by asking whether there was any absolute difference in the proportion of contrasts activating near those voxels (within 10 mm) for each emotion category v. the others. This was accomplished using c² analyses on the contingency table consisting of counts of study contrasts showing activation in or around these voxels vs. study contrasts without such activations for the target emotion category vs. other categories. This analysis yielded a series of statistical maps reflecting whether each voxel was more frequently activated in studies of each emotion category vs. the average of the others, irrespective of activations elsewhere in the brain.

Both density and c²analyses speak to whether increased activations in a set of voxels that are consistently associated with the experience or perception of instances of an emotion category are also functionally selective⁴ for that emotion category. A region that is functionally selective for instances of an emotion category would show voxels that are significant in both the density analysis and c² analysis. Functional specificity exists if voxels activated selectively for instances of one emotion category also never show increased activity during instances of any other emotion categories. We did not find evidence for functional specificity with respect to any emotion category in our analyses (i.e., every region that was activated for one emotion category was activated for at least one other category), so our findings only speak to functional selectivity.

4.1.3. Logistic regressions. Finally, in a third set of analyses we used a series of stepwise logistic regressions to ask which emotion categories and experimental methods predicted increased activity in regions of interest. We present the odds ratios for these regressions (in Table S6) or the percent increase in odds that a variable predicted increased activity in a brain area or no increase in a brain area (in Figure 6) ⁵. The logistic regressions speak to both consistency and specificity of increased brain activation. Consistency is observed when any variable significantly predicted increased activity in a given brain area. Specificity is observed when one variable significantly predicted increased activity in a given brain area but all others significantly predicted no increase in activity. If a variable was not a significant predictor, then it is sometimes associated with increased activity, and is sometimes not.

5. Testing Hypotheses of Brain-Emotion Correspondence

6. Conclusion

Over a century ago, William James wrote, “A science of the relations of mind and brain must show how the elementary ingredients of the former correspond to the elementary functions of the latter,” (p. 28, 1890). James believed that emotions, thoughts, and memories are folk categories with instances that do not require special brain centers. With respect to emotion, he wrote, “sensational, associational, and motor elements are all that [the brain] need contain” to produce the variety of mental states that correspond to our commonsense categories for emotion (cf., p. 473, James, 1890/1998). James’ view foreshadowed modern psychological constructionist models of the mind and the findings of our meta-analytic review, which are largely in agreement with this approach. Our findings are consistent with the idea that emotion categories are not natural kinds that are respected by the brain. The fact that some of the regions we report also appear in meta-analyses of other task domains (e.g., action simulation and perception; Grezes & Decety, 2001; autobiographical memory; Svoboda et al. 2006; decision-making; Krain et al. 2006; executive control; Owen et al. 2005; Wager & Smith, 2003; Wager et al. 2004; language; Vigneau et al. 2006; self-referential processing; Northoff et al. 2006) means that these regions are not specific to emotion per se, and are also involved in constituting other cognitive and perceptual events (for a discussion of domain general networks, see Dosenbach et al. 2006; Nelson, et al. 2010; Spreng et al. 2009; van Snellenberg & Wager, 2009). Such findings show that even categories like emotion, cognition, and perception are not respected by the brain (Barrett, 2009a; Duncan & Barrett, 2007; Pessoa, 2008).

In keeping with James’ predictions, our meta-analytic review did not find strong evidence for a locationist hypothesis of brain-emotion correspondence. In all instances where a brain region showed consistent increases in activation during instances of a discrete emotion category (e.g., the amygdala in instances of fear perception), this increase was not specific to that category, failing to support a key locationist assumption. Some brain regions showed functional selectivity for instances of certain emotion categories; these findings perhaps point to differences in the contents of mental states (e.g., instances of anger experience often involve approach motivation, instances of disgust perception often involve simulation of bodily activation, and instances of fear perception often involve detection of unusual and hence salient stimuli).

Our meta-analytic findings were relatively more consistent with the psychological operations that we have considered ingredients of emotion here and in other papers (e.g., Barrett, 2006b; 2009; Barrett, Lindquist & Gendron, 2007; Lindquist & Barrett, 2008; Kober et al. 2008; Wager et al. 2008). In Kober et al. (2008), we hinted at the existence of basic psychological operations in the psychological construction of emotion. In other theoretical discussions (Barrett, 2009) we explicitly hypothesized the need for mid-level scientific categories that describe the most basic psychological ingredients of the mind by referencing both biology and folk psychology when explaining how mental states like emotion experiences and perceptions arise (for a similar view, see Cacioppo et al., 2008). This paper is the first to investigate the extent to which brain regions associated with basic psychological domains show consistent increases in activation in neuroimaging studies of discrete emotion categories, despite a range of methodological variables. Of course, more work needs to be done to hone and refine our conceptions of the operations that are most psychological primitive and map them to networks in the brain, but this is a start.

Most notably, we observed consistent increases in activation in the brain regions implicated in conceptualization (simulation of prior episodic experiences), language (representation and retrieval of semantic concepts), and executive attention (volitional attention and working memory), suggesting that these more “cognitive” functions play a routine role in constructing experiences and perceptions of emotion. For instance, increased activation in DMPFC was observed when participants perceived instances of emotion on others’ faces. Increased activation in ATL was observed when participants focused on emotional stimuli. Increased activity in VLPFC occurred when participants focused on the affective content of feelings or perceived instances of emotion on another person’s face. Increased activity in DLPFC occurred when participants evaluated the emotional content of a stimulus. One interpretation of these findings is that they are merely the result of the types of psychological tasks participants are asked to perform in the scanner during neuroimaging studies of emotion (e.g., recall, labeling, response selection), and that due to the limits of neuroimaging these influences cannot be separated from an emotion itself. Yet, all data in our meta-analysis were derived from emotion v. neutral contrasts, meaning that, regardless of the task at hand, activation in these brain areas was greater when participants were experiencing or perceiving an emotion category than when they were in experiencing or perceiving in a neutral control state. Activity in these brain regions is thus integral to producing instances of emotion.

Our findings suggested the need to refine and add additional psychological operations to our model. Just as executive attention has been parsed into a set of distinguishable networks (e.g., Dosenbach et al. 2007; Corbetta & Shulman 2002; Corbetta, Patel & Shuman, 2008; Seeley et al. 2007), we might further refine core affect into a set of smaller networks that correspond to even more basic mechanisms. For example, we might find separable networks corresponding to approach vs. avoidance related states. Our findings hint that brain regions in the left prefrontal cortex might be candidates for a network involved in approach motivation because regions in left lateral PFC (including the anterior and mid-insula, VLPFC, DLPFC and OFC) were consistently observed during instances of the experience of anger. This hypothesis is consistent with a large body of EEG evidence associating L. PFC with the experience of instances of anger (Harmon-Jones & Allen, 1997; Harmon-Jones & Sigelman, 2001) and approach motivation more generally (Amodio, et al. 2008; Fox, 1991; Sutton & Davidson, 1997). Future meta-analytic investigations should investigate the degree to which L. PFC and subcortical regions supporting incentive salience (e.g., ventral tegmentum, amygdala, and aspects of the nucleus accumbens and ventral pallidum; see Berridge & Robinson, 2003) comprise a network for approach-related affect within the operation of core affect. We might also add ingredients for processing exteroceptive sensory sensations to our theoretical framework since visual cortex was one of the most frequently activated brain regions in our meta-analysis of discrete emotions. Exteroceptive sensory sensations are also important components of other types of mental states (e.g., perception, memory, judgments).

Table 3. Summary of Brain Regions Showing Consistent Increases in Activation During Mental States and Methodological Manipulations

Mode	Variable Experience of emotion Perception of emotion
Affect Emotion	High arousal emotions Unpleasant emotions Anger experience
	Anger perception
	Disgust experience
	Disgust perception
	Fear experience
	Fear perception

Happiness experience

Area

R. lOFC

7. Unifying the Mind

A psychological constructionist approach is not only a viable approach for understanding the brain basis of emotion, but it might also offer a new psychological ontology for a neuroscience approach to understanding the mind. If a psychological constructionist approach to the mind is right, then some of psychology’s time honored folk distinctions become phenomenological distinctions. This has implications for understanding a range of psychological phenomena, including decision-making, attention, visual perception, mental illness, and perhaps even consciousness more generally. Indeed, similar efforts are emerging in other psychological domains (Fuster, 2006; Poldrack, Halchenko & Hanson, 2009; Price & Friston, 2005; Warnick, LaPorte & Kalueff, 2010). According to a psychological constructionist view of the mind, emotion does not influence cognition during decision-making as one pool ball exerts influence on another. Instead the view suggests that core affect, conceptualization, and executive attention (and perhaps other psychological operations) cooperate to realize a behavioral outcome. If this is the case, then we might not assume that emotion and cognition battle it out in the brain when a person makes the moral decision to sacrifice one life to save many (e.g., Greene et al. 2004), or that consumer decisions are predicated on competing affective and rational representations (e.g., Knutson et al. 2007). Instead, we might assume that affect and executive attention are merely different sources of attention in the brain rather than processes that differ in kind (Barrett, 2009b; Vuilleumier & Driver, 2007). Feeling and seeing might not be as distinct as typically assumed (Barrett & Bar, 2009; Duncan & Barrett, 2007). Even conceptions about “internal” vs. “external” processing begin to break down when we take into account the fact that “internal” ingredients like affect and conceptualization shape the very way in which exteroceptive sensory input is realized as perceptions by the brain (Bar, 2009; Barrett & Bar, 2009). A psychological constructionist framework of the mind thus begins to break down the most steadfast assumptions of our commonsense categories. In so doing, it charts a different but exciting path forward for the science of the mind.

Acknowledgments

We thank Amitai Shenhav for his insights into the amygdala’s the role in uncertainty, Natasha Sarkisian for her advice on logistic regression and Kurt Gray for his help with Figure 6. We’d also like to thank James Russell, Elizabeth Kensinger, Hiram Brownell, Jerry Clore, and Stephan Hamann who commented on an earlier draft of this manuscript. This project was supported by a NSF Graduate Research Fellowship and a Harvard University Mind/Brain/Behavior Initiative Postdoctoral Fellowship to Kristen Lindquist, a NSF Graduate Research Fellowship to Hedy Kober, an NSF grant (NSF 0631637) and an NIMH grant (R01MH076136) to Tor Wager, and an NIH Director’s Pioneer Award (DP1OD003312), an NIA grant (R01 AG030311), and an ARI contract (W91WAW-08-C-0018) to Lisa Feldman Barrett. The views, opinions, and/or findings contained in this article are solely those of the authors’ and should not be construed as an official Department of the Army or DOD position, policy, or decision.

Notes

1. These hypotheses have been inspired, in large part, by behavioral neuroscience research in non-human animals that has carefully mapped the circuitry for behavioral adaptations that occur in response to specific environmental challenges (e.g., freezing, attack, vocalizations). One variant of a locationist view focuses on the circuitry for behavioral adaptations such as freezing, escaping, aggressing, etc. (e.g., LeDoux, 2008; Panksepp, 1998), and assume that one behavioral adaptation is at the core of each discrete emotion category. This one-to-one correspondence between a behavioral adaptation and a discrete emotion category has been challenged on the basis of existing research showing that mammals such as rats display a variety of behaviors based on what is most effective in a given context, however (for discussion, Barrett, 2009a; Barrett, Lindquist et al., 2007).
2. For instance, because the neurons within the amygdala are part of the neural reference space for discrete emotion, we can say with some certainly that the amygdala is likely to have increased activation when a person is experiencing or perceiving any emotion. This does not mean that the amygdala is necessary to each and every instance of emotion or even that it is specific to emotion, however. These ideas distinguish our approach from locationist accounts that assume that neurons within a given brain area (e.g., the amygdala) are consistently and specifically linked to a particular category of mental state (e.g., “fear”).
3. We only discuss those meta-analyses that compare multiple emotion categories.
4. Here we use the term “functionally selective” to mean that a brain area can have some preference for certain mental states, even if it is not specific to that mental state. Functional selectivity might occur because a brain area supports a more basic psychological operation that helps to construct a certain mental state (e.g., the amygdala supports detection of salient exteroceptive sensations and is functionally selective for instances of fear). Functional selectivity does not refer to specificity, however. A brain area might be functionally selective for one mental state or even one basic psychological operation in one instance and another state or operation in another instance. Functional selectivity is distinct from the concept of “selective influence” (cf. Sternberg, 2001), where a brain area being involved in one mental state (e.g., an instance of fear) but not another (e.g., an instance of anger) is taken as evidence of modularity.
5. For example, given that there is an increase in activation in the amygdala, the probability that a person is experiencing fear might be 0.7. The probability that he or she is experiencing another emotion (e.g., anger, disgust, happiness or sadness) is 1-0.7=0.3. The odds ratio = 0.7/0.3=2.33. This means that given increased amygdala activation, the odds are 2.33 to 1 that the person is experiencing fear. In this case, the experience of fear is 113% more likely to predict increased activation in the amygdala than any other emotion state.
1. These findings might explain the amgydala’s role in “fear learning” without assuming that the amygdala is specific to fear. In “fear learning,” for example, amygdala activity reflects orienting responses that occur when an organism learns to associate a neutral stimulus with an already
2. salient stimulus. The amygdala contributes to the production of the skin conductance responses (SCRs) (Laine et al. 2009) used to index “fear learning.” Amygdala responses are associated with SCRs that occur immediately following the onset of a conditioned stimulus, suggesting that the amygdala is particularly involved in attention during learning but perhaps not the formation of associations (Cheng et al. 2007; also see Blakeslee, 1979 and Spinks et al. 1984 for evidence that SCRs covary with changes in attention). This orienting account would also explain why amygdala activity is observed when animals learn to associate neutral stimuli with rewarding outcomes (e.g., Paton et al. 2006; for a review see Murray, 2007), why amygdala activity corresponds to evaluative goals in the presence of both positive and negative stimuli (e.g., Cunningham et al. 2008; Paton et al. 2006), and why stimulation of the amygdala facilitates orienting responses like startle (Rosen & Davis, 1988). Together, these findings make it clear why the amygdala is so ubiquitously involved in mammalian social behavior (i.e., male and female sexual behavior, maternal behavior, aggression; see Newman, 1999).
6. Over 90% (53/57) of study contrasts assessing fear perception in our database used startled faces that are unfamiliar to college students (who are typically participants in neuroimaging studies of healthy samples) (Whalen et al. 2001) and highly arousing (e.g., Russell & Bullock, 1986). About 35% (15/43) of study contrasts assessing the experience of disgust presented participants with images that were novel (i.e., infrequently experienced in the industrialized world) and highly arousing (i.e., containing contamination, mutilated body parts, maggots, etc.).
7. EEG findings do not associate instances of anger with OFC specifically, probably because EEG does not easily pick up activity in the orbital sector.
8. mOFC and sACC, which are more generally part of VMPFC, were part of the neural reference space and are reported in separate sections. Aspects of VMPFC that do not include mOFC/sACC were part of the neural reference space, but were not significant at the thresholds we report in this manuscript.
9. In some theoretical treatments of emotion, emotion regulation is thought to be a separate psychological event from emotion generation, with distinctive neural correlates; in a psychological constructionist approach, however, the processes are the same because there is no conceptual distinction between generation and regulation (Gross & Barrett, in press).
10. “Resting state” or “default” networks are evidenced as correlations between low-frequency signals in fMRI data that are recorded when there is no external stimulus or task. These networks are thought to be intrinsic in the human brain. For a review of intrinsic networks and their function, see Deco, Jirsa and McIntosh, 2011.

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