4.1. Analysis strategy

In the present article, we expanded upon our initial meta-analytic efforts to directly compare the locationist versus the psychological constructionist approach for neuroimaging studies of discrete emotion. A detailed description of our meta-analytic methods and Figure S1 are included in the supplementary materials (available at: http://www.journals.cambridge.org/bbs2012008). 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 (see Tables S1 and S2 in supplementary materials for details on the inclusion criteria and database; available at: http://www.journals.cambridge.org/bbs2012008). We also conducted a number of statistical analyses with the potential to yield evidence in favor of a locationist account (outlined in the next section).

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 category 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, and so forth, 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 (Fig. 4; see also Table S3 in supplementary materials, available at: http://www.journals.cambridge.org/bbs2012008) closely resembles the one reported in Kober et al. (Reference Kober, Barrett, Joseph, Bliss-Moreau, Lindquist and Wager2008), 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 in others.

Figure 4. The Neural Reference Space for Discrete Emotion. The neural reference space (phrase coined by Edelman [1989]) is the set of brain regions consistently activated across all studies assessing the experience or perception of anger, disgust, fear, happiness and sadness (i.e. the superordinate category emotion). Brain regions in yellow exceeded the height threshold (p<05) and regions in orange exceeded the most stringent extent-based threshold (p<001). Regions in pink and magenta correspond to lesser extent-based thresholds and are not discussed in this article. Cortex is grey, the brainstem and nucleus accumbens are green, the amygdala is blue and the cerebellum is purple. A color version of this image can be viewed in the online version of this target article at http://www.journals.cambridge.org/bbs.

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 in the supplementary materials, available at http://www.journals.cambridge.org/bbs2012008) or the percent increase in odds that a variable predicted either increased activity in a brain area or no increase in a brain area (in Fig. 5).Footnote ⁴ 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.

Figure 5. Logistic Regression Findings. Selected results from the logistic regressions are presented (for additional findings, see Table S6 in supplementary materials). Circles with positive values represent a 100% increase in the odds that a variable predicted an increase in activity in that brain area. Circles with negative values represent a 100% increase in the odds that a variable predicted there would not be an increase in activity in that brain area. Legend: Blue lines: left hemisphere; Green lines: right hemisphere. Arrowheads: % change in odds is greater than values represented in this figure. Abbreviations: OFC: orbitofrontal cortex; DLPFC: dorsolateral prefrontal cortex; ATL: anterior temporal lobe; VLPFC: ventrolateral prefrontal cortex; DMPFC: dorsomedial prefrontal cortex; aMCC: anterior mid-cingulate cortex; sAAC: subgenual ACC. A color version of this image can be viewed in the online version of this target article at http://www.journals.cambridge.org/bbs.

5.1. The amygdala

According to a locationist hypothesis, the amygdala (Fig. 1, yellow) is either the brain locus of fear or is the most important hub in a fear circuit. This amygdala-fear hypothesis was most clearly popularized by behavioral neuroscience work showing that the amygdala (in particular, the central nucleus) supports the cardiovascular changes that occur when rats freeze or startle in response to tones previously paired with shock (called “fear learning”: LeDoux et al. Reference LeDoux, Sakaguchi and Reis1983; Reference LeDoux, Sakaguchi, Iwata and Reis1985; Reference LeDoux, Ciccetti, Xagoraris and Romanski1990; for reviews see Fanselow & Poulous 2005; Fendt & Fanselow Reference Fendt and Fanselow1999; LeDoux Reference LeDoux2007; Öhman Reference Öhman2009; and “fear potentiated startle”: Davis Reference Davis1992; Hitchcock & Davis Reference Hitchcock and Davis1986; Reference Hitchcock and Davis1987; see Davis et al. Reference Davis, Amaral and Winslow2008; Fendt & Fanselow Reference Fendt and Fanselow1999). Electrical stimulation of the amygdala elicits defensive behavior in rats (e.g., retreat; Maskati & Zbrozyna Reference Maskati and Zbrozyna1989) and enhances startle to acoustic stimuli (Rosen & Davis Reference Rosen and Davis1988). The amygdala-fear hypothesis was further strengthened by evidence that humans show increased amygdala activity to neutral tones that have been previously paired with noxious noise blasts (i.e., “fear learning”; LaBar et al. Reference LaBar, Gatenby, Gore, LeDoux and Phelps1998). Individuals with amygdala lesions (LaBar et al. Reference LaBar, LeDoux, Spencer and Phelps1995) or atrophy (Bechara et al. Reference Bechara, Tranel, Damasio, Adolphs, Rockland and Damasio1995) show impaired skin conductance responses during “fear learning” and have difficulty perceiving instances of fear in voices (Brierley et al. Reference Brierley, Medford, Shaw and David2004; Scott et al. Reference Scott, Young, Calder, Hellawell, Aggleton and Johnson1997, but see, Adolphs & Tranel Reference Adolphs and Tranel1999; Anderson & Phelps Reference Anderson and Phelps1998), bodies (Sprengelmeyer et al. Reference Sprengelmeyer, Young, Schroeder, Grossenbacher, Federlein, Büttner and Przuntek1999; but see, Atkinson et al. Reference Atkinson, Heberlein and Adolphs2007), and startled faces with wide eyes (e.g., Adolphs et al. Reference Adolphs, Tranel, Damasio and Damasio1994; Reference Adolphs, Tranel, Damasio and Damasio1995; Reference Adolphs, Tranel, Hamann, Young, Calder, Phelps, Anderson, Lee and Damasio1999; although see, Adolphs et al. Reference Adolphs, Gosselin, Buchanan, Tranel, Schyns and Damasio2005; Tsuchiya et al. Reference Tsuchiya, Moradi, Felsen, Yamazaki and Adolphs2009). An individual with bilateral amygdala lesions failed to report fearful experiences when placed in close contact with snakes, spiders, or when startled (Feinstein et al. Reference Feinstein, Adolphs, Damasio and Tranel2011; although see, Anderson & Phelps Reference Anderson and Phelps2002). Finally, the amygdala is implicated in psychopathology involving the experience of anxiety in humans (for a review, see Damsa et al. Reference Damsa, Kosel and Moussally2009; for a meta-analytic review, see Etkin & Wager Reference Etkin and Wager2007).

According to a psychological constructionist view, the amygdala is part of the distributed network that helps to realize core affect (Fig. 2, panel D, bright pink) because it is involved in signaling whether exteroceptive sensory information is motivationally salient (for similar views see Adolphs Reference Adolphs2008; Reference Adolphs2009; Duncan & Barrett Reference Duncan and Barrett2007; Pessoa Reference Pessoa2010b; Pessoa & Adolphs Reference Pessoa and Adolphs2010; Sander et al. Reference Sander, Grafman and Zalla2003; Whalen Reference Whalen2007; Whalen Reference Whalen1998). The amygdala is most likely to be active when the rest of the brain cannot easily predict what sensations mean, what to do about them, or what value they hold in that context. Salient objects or events influence an organism's body state in a way that can be experienced as core affective feelings (Barrett & Bliss-Moreau Reference Barrett and Bliss-Moreau2009). They can also cause the amygdala to signal to other parts of the brain to sustain processing so that uncertainty about the stimulus can be resolved (Whalen Reference Whalen2007). As a result, affect can be considered a source of attention in the brain (Barrett & Bar Reference Barrett and Bar2009; Duncan & Barrett Reference Duncan and Barrett2007; Pessoa Reference Pessoa2008; Reference Pessoa2010b; Vuilleumier Reference Vuilleumier2005; Vuilleumier & Driver Reference Vuilleumier and Driver2007).

From a psychological constructionist point of view, fear-inducing stimuli might fall into the class of uncertain and therefore salient stimuli, but the amygdala is not specific to the category fear. Consistent with this view, the amygdala is routinely implicated in orienting responses to motivationally relevant stimuli (Holland & Gallagher Reference Holland and Gallagher1999). Novel stimuli (e.g., Blackford et al. Reference Blackford, Buckholtz, Avery and Zald2010; Breiter et al. Reference Breiter, Etcoff, Whalen, Kennedy, Rauch, Buckner, Strauss, Hyman and Rosen1996; Moriguchi et al. Reference Moriguchi, Negreira, Weirerich, Dautoff, Dickerson, Wright and Barrett2010; Schwartz et al. Reference Schwartz, Wright, Shin, Kagan, Whalen, McMullin and Rausch2003; Weierich et al. Reference Weierich, Wright, Negreira, Dickerson and Barrett2010; Wilson & Rolls Reference Wilson and Rolls1993; Wright et al. Reference Wright, Martis, Schwartz, Shin, Fischer, McMullin and Rausch2003; Reference Wright, Wedig, Williams, Rauch and Albert2006; Reference Wright, Negreira, Gold, Britton, Williams and Barrett2008), uncertain stimuli (e.g., Herry et al. Reference Herry, Bach, Esposito, Di Salle, Perrig, Scheffler, Lüthi and Seifritz2007), and unusual stimuli (e.g., Blackford et al. Reference Blackford, Buckholtz, Avery and Zald2010) robustly activate the amygdala and produce cardiovascular responses associated with affective changes (Mendes et al. Reference Mendes, Blascovich, Hunter, Lickel and Jost2007). Amygdala lesions disrupt normal responses to novelty and uncertainty in mammals (e.g. Bliss-Moreau et al. Reference Bliss-Moreau, Toscano, Baumann, Mason and Amaral2010; Burns et al. Reference Burns, Annett, Kelley, Everitt and Robbins1996; Mason et al. Reference Mason, Capitanio, Machado, Mendoza and Amaral2006; Missilin & Ropartz Reference Missilin and Ropartz1981; Nachman & Ashe Reference Nachman and Ashe1974; for reviews, see Knight & Grabowecky 1999; Petrides Reference Petrides2007). Individuals with amygdala lesions do not automatically allocate attention to aversive stimuli (Anderson & Phelps Reference Anderson and Phelps2001) and socially relevant stimuli (Kennedy & Adolphs Reference Kennedy and Adolphs2010), as do individuals with intact amygdalae. Amygdala responses habituate rapidly (Breiter et al. Reference Breiter, Etcoff, Whalen, Kennedy, Rauch, Buckner, Strauss, Hyman and Rosen1996; Büchel et al. Reference Büchel, Dolan, Armony and Friston1999; Fischer et al. Reference Fischer, Wright, Whalen, McInerney, Shin and Rauch2003; Whalen et al. Reference Whalen, Kagan, Cook, Davis, Kim, Polis, McLaren, Somerville, McLean, Maxwell and Johnstone2004; Wright et al. Reference Wright, Fischer, Whalen, McInerney, Shin and Rauch2001), suggesting that the amygdala is involved in attention to salient stimuli, but calling into question the idea that the amygdala is necessary to fear per se (for a similar point, see Adolphs Reference Adolphs2008; Reference Adolphs2010; Pessoa & Adolphs Reference Pessoa and Adolphs2010; Todd & Anderson Reference Todd and Anderson2009; Whalen Reference Whalen2007).Footnote ⁵

The amygdala's role in detecting motivationally salient stimuli would also explain why increased amygdala activity is observed in instances that do not involve the experience of fear, such as when stimuli are experienced as subjectively arousing (e.g., Bradley et al. Reference Bradley, Codispoti, Cuthbert and Lang2001; Weierich et al. Reference Weierich, Wright, Negreira, Dickerson and Barrett2010), intense (e.g., Bach et al. Reference Bach, Schachinger, Neuhoff, Esposito, Di Salle, Lehmann, Herdener, Scheffler and Seifrit2008), emotionally “impactful” (e.g., Ewbank et al. Reference Ewbank, Barnard, Croucher, Ramponi and Calder2009), or valuable (Jenison et al. Reference Jenison, Rangel, Oya, Kawasaki and Howard2011). Moreover, not all instances of fear are accompanied by increased amygdala activity (for a review, see Suvak & Barrett Reference Suvak and Barrett2011). For example, some behaviors that rats perform in dangerous contexts are not amygdala-dependent (e.g., avoiding the location of a threat: Vazdarjanova & McGaugh Reference Vazdarjanova and McGaugh1998; “defensive treading,” where bedding is kicked in the direction of the threat: Kopchia et al. Reference Kopchia, Altman and Commissaris1992). In humans, threatening contexts devoid of salient visual stimuli (e.g., preparing to give a speech in front of an audience), actually produce deactivatations in the amygdala (Wager et al. Reference Wager, van Ast, Hughes, Davidson, Lindquist and Ochsner2009a; Reference Wager, Waugh, Lindquist, Noll, Fredrickson and Taylor2009b). Moreover, electrical stimulation to the amygdala produces a range of experiences in humans, calling into question the idea that the amygdala is specifically linked to instances of fear (Bancaud et al. Reference Bancaud, Brunet-Bourgin, Chauvel and Halgren1994; Gloor Reference Gloor1990; Halgren et al. Reference Halgren, Walter, Cherlow and Crandall1978).

Our meta-analytic findings were inconsistent with a locationist hypothesis of amygdala function but were more consistent with the psychological constructionist hypothesis. Our density analyses revealed that, as compared to other brain regions, voxels within both amygdalae had more consistent increases in activation during instances of fear perception than during the perception of any other emotion category (Table 1). These voxels were not functionally specific for instances of perceiving fear, however. An insignificant χFootnote ² analysis revealed that the voxels with consistent increases in activation during instances of fear perception were equally likely to have increased activity during instances of other emotion categories (see Fig. 6 for the proportion of study contrasts in the database for each emotion category that are associated with increased activity in right [R] amygdala; see Fig. S2 in the supplementary material, available at http://www.journals.cambridge.org/bbs2012008, for left [L] amygdala). Furthermore, instances of fear experience did not show a consistent increase in activation in either amygdala when compared to what would be expected by chance in other regions of the brain. Yet, as compared to other brain regions, voxels within bilateral amygdala had more consistent increases in activation during instances of disgust experience than during the experience of other emotion categories (Table 1). A χFootnote ² analysis revealed that these voxels were functionally selective for of the experience of disgust, as there was more likely to be increased activity in those voxels during instances of disgust experience than during the experience of anger, fear, happiness or sadness (Table 2). Those voxels were not functionally specific to instances of disgust experience, however (Fig. 6; Fig. S2). Finally, as compared to other brain regions, a voxel in L. amygdala had more consistent increases in activation during instances of sadness perception than during the perception of other emotion categories (Table 1). An insignificant χFootnote ² analysis revealed that this voxel was not functionally selective for instances of sadness, however.

Figure 6. Proportion of Study Contrasts with Increased Activation in Four Key Brain Areas. The y-axes plot the proportion of study contrasts in our database that had increased activation within 10mm of that brain area. The x-axes denote the contrast type separated by experience (exp) and perception (per). All brain regions depicted are in the right hemisphere. See Figures S2 and S3 in supplementary materials, available at http://www.journals.cambridge.org/bbs2012008, for additional regions. A color version of this image can be viewed in the online version of this target article at http://www.journals.cambridge.org/bbs.

Table 1. Brain Regions with a Consistent Increase in Activity Associated with the Experience or Perception of Discrete Emotion Categories in Density Analyses

Table 2. Brain Regions with a Consistent Increase in Activity Associated with the Experience or Perception of Discrete Emotion Categories in χFootnote ² Analyses

Our logistic regressions confirmed and expanded upon our density and χFootnote ² findings. There was more likely to be increased activity in the L. amygdala when participants were perceiving instances of fear or experiencing instances of disgust than when perceiving or experiencing any other emotion categories (Fig. 5; Table S6). These findings are consistent with the psychological constructionist hypothesis that the amygdala responds to salient perceptual stimuli because contrasts in our database that assessed the perception of fear and experience of disgust tended to use visual stimuli that are novel or unfamiliar to participants.Footnote ⁶ Findings for the R. amygdala also supported a psychological constructionist view. Increases in activity in the R. amygdala were likely when participants were experiencing or perceiving instances of any highly arousing emotion category (i.e., anger, disgust, fear) (Fig. 5; Table S6). There was likely to be no increase in activity in the L. amygdala when participants were focusing on their internal state (i.e., when emotion experience was induced via recall of a personal event and mental imagery; Fig. 5; Table S6). This finding replicates prior meta-analytic evidence (Costafreda et al. Reference Costafreda, Brammer, David and Fu2008) and is consistent with our hypothesis that the amygdala responds preferentially to salient exteroceptive (vs. interoceptive) sensations.

5.2. The anterior insula

Locationist accounts hypothesize that the anterior insula (Fig. 1, green) is the brain basis of disgust (e.g., Jabbi et al. Reference Jabbi, Bastiaansen and Keysers2008; Wicker et al. Reference Wicker, Keysers, Plailly, Royet, Gallese and Rizzolati2003; for reviews, see Calder et al. Reference Calder, Lawrence and Young2001; Calder Reference Calder2003) based on the belief that disgust evolved from a primitive food rejection reflex (Rozin et al. Reference Rozin, Haidt, McCauley, Lewis and Havilland-Jones2000) or bodily aversion to disease-threat (e.g., Curtis et al. Reference Curtis, Aunger and Rabie2004). Individuals with damage to the anterior insula and basal ganglia have difficulty perceiving instances of disgust in facial and vocal caricatures (Adolphs et al. Reference Adolphs, Tranel and Damasio2003; Calder et al. Reference Calder, Keane, Manes, Antoun and Young2000). They also report experiencing less disgust in response to scenarios about body products, envelope violation, and animals that typically evoke disgust in people with intact insulas (Calder et al. Reference Calder, Keane, Manes, Antoun and Young2000). Individuals with neurodegenerative diseases affecting the insula and basal ganglia (such as Huntington's and Parkinson's disease) also show diminished experiences of disgust to foul smelling odors (Mitchell et al. Reference Mitchell, Heims, Neville and Rickards2005) and have difficulty perceiving instances of disgust in the faces of others (e.g., Kipps et al. Reference Kipps, Duggins, McCusker and Calder2007; Sprenglemeyer et al. 1996; 1998; Suzuki et al. Reference Suzuki, Hoshino, Shigemasu and Kawamura2006; see Calder et al. Reference Calder, Lawrence and Young2001; Sprengelmeyer Reference Sprengelmeyer2007, for reviews), although the specificity of these findings remains in question (e.g., Calder et al. Reference Calder, Keane, Young, Lawrence, Mason and Barker2010; Milders et al. Reference Milders, Crawford, Lamb and Simpson2003). Patients who received electrical stimulation to the anterior insula reported visceral sensations consistent with (but not specific to) the experience of disgust (e.g., sensations in the stomach or throat, smelling or tasting something bad, nausea; Penfield & Faulk 1955).

In a psychological constructionist hypothesis, the anterior insula plays a key role in representing core affective feelings in awareness (Fig. 2, panel D, dark pink). The anterior insula is thought to be involved in the awareness of bodily sensations (Craig Reference Craig2002) and affective feelings (Craig Reference Craig2009). Sometimes sensations from the body are experienced as physical symptoms, but more often they are experienced as states that have some hedonic tone and level of arousal. Sometimes those affective feelings are experienced as emotion. To the extent that brain states corresponding to instances of disgust represent a stimulus's consequence for the body, then the anterior insula will show increased activation. Indeed, a key ingredient in the mental states labeled “disgust” is likely a representation of how an object will affect the viscera. In support of a psychological constructionist view, anterior insula activation is observed in a number of tasks that involve awareness of body states, but not disgust per se. The anterior insula shows increased activation during awareness of body movement (e.g., Tsakiris et al. Reference Tsakiris, Hesse, Boy, Haggard and Fink2007), gastric distention (e.g., Wang et al. Reference Wang, Tomasi, Backus, Wang, Telang, Geliebter, Korner, Bauman, Fowler, Thanos and Volknow2008), and orgasm (e.g., Ortigue et al. Reference Ortigue, Grafton and Bianchi-Demicheli2007). Electrical stimulation of the insula produces sensations consistent with the category disgust, but it also produces a range of other visceral sensations including feelings of movement, twitching, warmth and tingling in the lips, tongue, teeth, arms, hands, and fingers (Penfield & Falk Reference Penfield and Falk1955). Dorsal anterior insula is also a hub in a large-scale network involved in what has been called a ventral attention system (Corbetta & Shulman Reference Corbetta and Shulman2002, Corbetta et al. Reference Corbetta, Patel and Shulman2008) that guides attention allocation and orienting (e.g., Eckert et al. Reference Eckert, Menon, Walczak, Ahlstrom, Denslow, Horowitz and Dubno2009). These findings again point to the idea that body-based sensory signals constitute a source of attention in the brain.

Our meta-analytic findings were inconsistent with the locationist account that the anterior insula is the brain seat of disgust but were more consistent with the psychological constructionist account that insula activity is correlated with interoception and the awareness of affective feelings. Our density analyses revealed that as compared to other brain regions, voxels within the right [R.] anterior insula had more consistent increases in activation during instances of disgust perception than during the perception of any other emotion category (Table 1). Our χFootnote ² analysis revealed that only four of the voxels identified in the density analysis showed functional selectivity for instances of disgust perception (Table 2), however, and increased activity in R. insula was not specific to instances of disgust perception (Fig. 6). Our logistic regression findings for the R. anterior insula were consistent with the psychological constructionist hypothesis that the insula supports representation of core affective feelings. Increased activity in R. anterior insula was likely when participants were explicitly evaluating their feelings and representing them in awareness (Fig. 5, Table S6). Instances of disgust perception might consistently involve increased activation in the insula because people are more likely to simulate visceral states (such as those associated with the gut and food rejection) when perceiving facial behaviors characterized by a wrinkled nose and curled lip (i.e., oral revulsion; Angyal Reference Angyal1941; see also, Rozin et al. Reference Rozin, Haidt, McCaule, Lewis, Haviland-Jones and Barrett2008; von dem Hagen et al. Reference von dem Hagen, Beaver, Ewbank, Keane, Passamonti, Lawrence and Calder2009).

As compared to other brain regions, a greater spatial extent of voxels within the left [L.] anterior insula had consistent increases in activation during instances of disgust experience than during the experience of any other emotion category (Table 1). As compared to other brain regions, two voxels in L. anterior insula also had more consistent increases in activation during instances of anger experience than during the experience of any other emotion (Table 1; only one voxel showed functional selectivity, see Table 2). Our logistic regressions replicated this general finding. Increased activity in L. anterior insula was more likely when participants were experiencing an instance of anger than when they were experiencing any other emotion category (Fig. 5; Table S6). These findings, along with subsequent findings (see sect. 5.3 for the orbitofrontal cortex, sect. 5.6 for the anterior temporal lobe and ventrolateral prefrontal cortex, and 5.7 for the dorsolateral prefrontal cortex) suggest that instances of anger are associated with increased activity in a broad set of areas in the left frontal and temporal lobes.

5.3. The orbitofrontal cortex

Locationist accounts link the orbitofrontal cortex (OFC) to anger (Fig. 1, rust), although the OFC is a large structure and has admittedly been linked to many other psychological phenomena. Primary support for the OFC-anger hypothesis derives from prior meta-analytic reviews of the neuroimaging literature (Murphy et al. Reference Murphy, Nimmo-Smith and Lawrence2003; Vytal & Hamann Reference Vytal and Hamann2010). Studies using electroencephalography (EEG) also associate instances of anger with the prefrontal cortex (PFC).Footnote ⁷ Using EEG, activity in the left PFC is associated with instances of anger experience in response to an insult (Harmon-Jones & Sigelman Reference Harmon-Jones and Sigelman2001) and with the personality disposition to experience angry feelings (Harmon-Jones & Allen Reference Harmon-Jones and Allen1998). Other evidence for an OFC-anger hypothesis is more circumstantial. For instance, there is a body of evidence linking the OFC to aggression. It is far from clear that aggression is an unambiguous index of the entire category of anger, however. Nonhuman animals aggress in a number of different contexts (e.g., maternal aggression, sexual aggression, predatory aggression, defensive aggression; Moyer Reference Moyer1968); only some of which are associated with the concept called “anger” in English. Humans do a number of things in anger, only some of which constitute aggression. With that caveat, there is certainly evidence linking increased activity in the OFC to aggression. EEG activity in the left PFC is associated with an increased tendency to retaliate towards another person following an insult (by allocating him or her a dose of unpleasant hot sauce in a putative taste test; Harmon-Jones & Sigelman Reference Harmon-Jones and Sigelman2001). Aggressive behavior in rats is associated with increased activity in the ventral forebrain (including the OFC) (Ferris et al. Reference Ferris, Stolberg, Kulkarni, Murugavel, Blanchard, Blanchard, Febo, Brevard and Simon2008). Some lesion evidence is consistent with the idea that the OFC produces aggression in monkeys, because OFC lesions reduce aggression (towards humans: Butter & Snyder Reference Butter and Snyder1972; Kamback Reference Kamback1973; towards other monkeys: Raleigh et al. Reference Raleigh, Steklis, Ervin, Kling and McGuire1979). The majority of lesion studies find that monkeys (e.g., Deets et al. Reference Deets, Harlow, Singh and Blomquist1970; Machado & Bachevalier Reference Machado and Bachevalier2006; Raleigh et al. Reference Raleigh, Steklis, Ervin, Kling and McGuire1979) and rats (de Bruin et al. Reference de Bruin, Van Oyen and Van De Poll1983) are more aggressive towards conspecifics following OFC lesions, however. Similarly, electrical stimulation of the lateral OFC (lOFC; in cats: Siegel et al. Reference Siegel, Edinger and Dotto1975) and the medial OFC (mOFC; in cats: Siegel et al. Reference Siegel, Edinger and Lowenthal1974; and in rats: de Bruin Reference de Bruin1990) inhibits, rather than causes, aggressive behavior. Humans with lesions in the ventromedial PFC (which contains the OFC) become frustrated more easily and engage in more verbal (but not physical) aggression than do neurologically intact subjects (Grafman et al. Reference Grafman, Schwab, Warden, Pridgen, Brown and Salazar1996). Psychopathy and antisocial disorder are marked by increased aggression and correspond to structural (e.g., Raine et al. Reference Raine, Lencz, Bihrle, LaCasse and Colletti2000) and functional (e.g., Glenn et al. Reference Glenn, Raine and Schug2009; Harenski et al. Reference Harenski, Kim and Hamann2009) changes to the mOFC (Yang & Raine Reference Yang and Raine2009). Fewer studies have linked the lOFC to aggressive behavior in humans, but one study found that individuals with borderline personality disorder who have lowered baseline lOFC (BA 47) activity are more likely to aggress against others (Goyer et al. Reference Goyer, Konicki, Schulz and Silk1994).

A psychological constructionist view hypothesizes that portions of the OFC play a role in core affect as a site that integrates exteroceptive and interoceptive sensory information to guide behavior. Together, sensory information from the world and sensory information from the body guide an organism's response to the environment and allow it to engage in behavior that is well tuned to the context (defined both by the external surroundings and the organism's goals). With the lOFC's connections to sensory modalities (e.g., Barbas Reference Barbas1988; Rolls Reference Rolls1999, see Kringelbach & Rolls Reference Kringelbach and Rolls2004) and the mOFC's connections to areas involved in visceral control (e.g., Carmichael & Price Reference Carmichael and Price1995; Eblen & Graybiel Reference Eblen and Graybiel1995; Ongür & Price 1998; Reference Öngür and Price2000; Rempel-Clower & Barbas Reference Rempel-Clower and Barbas1998; see Kringelbach & Rolls [2004] for a review), the OFC is anatomically well suited to perform this role. We are not claiming that this is the OFC's specific function, but only that it is a brain region that is important to realizing this function. Consistent with the idea that the OFC unites internal and external sensory information, the lOFC and the mOFC have been linked to associative learning (Rolls et al. Reference Rolls, Hornak, Wade and McGrath1994; Reference Rolls, Critchley, Mason and Wakeman1996) decision making (e.g., Bechara et al. Reference Bechara, Tranel, Damasio and Damasio1996; Reference Bechara, Tranel and Damasio2000; Koenigs et al. Reference Koenigs, Young, Adolphs, Tranel, Cushman, Hauser and Damasio2007) and reversal learning, in which the reward values associated with choice options are reversed and animals must learn the current reward value (Chudasama & Robbins Reference Chudasama and Robbins2003; Hornak et al. Reference Hornak, O'Doherty, Bramham, Rolls, Morris, Bullock and Polkey2004; Rudebeck & Murray Reference Rudebeck and Murray2008). The inability to properly integrate exteroceptive and interoceptive information will result in behavior that is inappropriate to that context, explaining the altered non-aggressive social behavior (e.g., Beer et al. Reference Beer, John, Scabini and Knight2003; Eslinger & Damasio Reference Eslinger and Damasio1985; Saver & Damasio Reference Saver and Damasio1991; see Damasio et al. Reference Damasio, Tranel and Damasio1990) and aggression (Grafman et al. Reference Grafman, Schwab, Warden, Pridgen, Brown and Salazar1996) observed in individuals with OFC damage.

Our meta-analytic findings were inconsistent with the locationist hypothesis that the OFC is the brain seat of anger. As compared to voxels within other brain regions, voxels within the OFC did not have more consistent increases during instances of anger experience or perception than during any other emotion category. Rather, as compared to voxels within other brain regions, voxels within the left lOFC had more consistent increases in activation during instances of disgust experience than during the experience of other emotion categories (Table 1). Voxels within the right lOFC, as compared to voxels within other brain regions, had more consistent increases in activation during instances of disgust perception than during the perception of other emotion categories (Table 1). χFootnote ² analyses indicated that there was some functional selectivity for instances of disgust experience and perception in the voxels in the right and left lOFC that were respectively identified in the density analysis. Activity in the right and left lOFC was not specific to instances of disgust experience or perception, however (Fig. 6; Fig. S2). Our logistic regressions confirmed that when participants were perceiving an instance of disgust, there was more likely to be increased activity in the right lOFC than when participants were perceiving instances of any other emotion category (Fig. 5; Table S6).

Our logistic regressions revealed that increased activity in the left lOFC was more likely when participants were experiencing instances of anger than when experiencing instances of any other emotion category (Fig. 5; Table S6). Although in and of itself, this finding provides partial support for the OFC-anger hypothesis, our other meta-analytic findings indicate that increased activity in the left hemisphere during instances of anger is not restricted to the OFC, or even the prefrontal cortex (see sect. 5.2, “The anterior insula,” sect. 5.6, “Anterior temporal lobe and ventrolateral prefrontal cortex,” and sect. 5.7, “Dorsolateral prefrontal cortex”). Additionally, our logistic regressions revealed that increased activity in the left and right lOFC was likely when participants were experiencing a range of exteroceptive (auditory stimuli, visual pictures) and interoceptive (experience or perception of high-arousal core affect) sensations (Fig. 5; Table S6). This finding is consistent with the psychological constructionist hypothesis that OFC plays a more general role in integrating heteromodal sensations.

5.4. The anterior cingulate cortex

Locationist accounts hypothesize that pregenual anterior cingulate cortex (pACC; BAs 24, 32) and subgenual anterior cingulate cortex (sACC; BA 25) are the brain basis of sadness (Fig. 1, blue). The pACC and sACC have known affective function and are thought to instantiate the visceromotor responses observed during classical conditioning, pain, and affective behaviors (Devinksy et al. 1995; Vogt Reference Vogt2005). The ACC-sadness hypothesis, like the OFC-anger hypothesis, derives support from prior meta-analyses of the neuroimaging literature (e.g., Murphy et al. Reference Murphy, Nimmo-Smith and Lawrence2003; Phan et al. Reference Phan, Wager, Taylor and Liberzon2002). In the behavioral neuroscience literature, pACC has been linked to sadness because of its role in producing the vocalizations that infant animals make when separated from their mother (e.g., MacLean & Newman Reference MacLean and Newman1988; see Panksepp Reference Panksepp1998; Reference Panksepp2007); the link between infant vocalizations and unpleasant affect are in question, however (Blumberg & Sokoloff Reference Blumberg and Sokoloff2001). One study in humans found that pACC lesions (including lesions to dorsomedial prefrontal cortex) produce hypersensitivity and an increased tendency to cry at sad events (Hornak et al. Reference Hornak, Bramham, Rolls, Morris, O'Doherty, Bullock and Polkey2003). If the pACC were involved in instantiating instances of sadness, then lesions to this structure should abolish the tendency to cry at sad events. These findings are therefore more consistent with the idea that pACC regulates instances of sadness. Finally, pACC is implicated in pain, perhaps because it supports the feeling of “suffering” (cf. Vogt Reference Vogt2005). The sACC, on the other hand, has been linked to sadness because of its role in depression. Clinical depression is marked by structural and functional changes in sACC (see Gotlib & Hamilton [2008] for a review), although clinical depression involves many symptoms above and beyond the experience of sadness (Coyne Reference Coyne1994). Electrical stimulation of the sACC relieves intractable depression by reducing feelings of apathy and anhedonia, normalizing sleep disturbances, and decreasing gross motor impairments (e.g., Mayberg et al. Reference Mayberg, Lozano, Voon, McNeely, Seminowicz, Hamani, Schwalb and Kennedy2005).

Our psychological constructionist hypothesis draws on the neuroscience literature showing that pACC, sACC, and the more dorsal anterior midcingulate cortex (aMCC) (Vogt Reference Vogt, Vogt and Gabriel1993; Vogt et al. Reference Vogt, Berger and Derbyshire2003) take part in distinct psychological operations related to realizing core affect. In our view, the pACC and sACC (along with the adjacent posterior mOFC) are cortical sites for visceral regulation that help to realize a core affective state during motivated action (Devinksy et al. 1995) (Fig. 2, panel B, light pinks). We would therefore predict increased activation in pACC and sACC across a variety of emotional instances. The hypothesized role of sACC in regulating somatovisceral states could explain why sACC is involved in the affective changes that accompany both depression (e.g., Drevets et al. 1992; see Gotlib & Hamilton Reference Gotlib and Hamilton2008) and mania (e.g., Fountoulakis et al. Reference Fountoulakis, Giannakopoulos, Kövari and Bouras2008), and why electrical stimulation of this region helps to relieve chronic depression (Mayberg, et al. Reference Mayberg, Lozano, Voon, McNeely, Seminowicz, Hamani, Schwalb and Kennedy2005). The aMCC (Fig. 2, panel B, dusty pink) is hypothesized to play a role in executive attention and motor engagement during response selection (Mansouri et al. Reference Mansouri, Tanaka and Buckley2009; Rushworth et al. Reference Rushworth, Buckley, Behrens, Walton and Bannerman2007). In this view, aMCC delivers sources of exteroceptive sensory information (from thalamic projections; Barbas et al. Reference Barbas, Henion and Dermon1991) and internal sensory information (from the insula; Mesulam & Mufson Reference Mesulam and Mufson1982) to direct attention and motor responses (via projections to lateral PFC and the supplementary motor area; e.g., Barbas & Pandya Reference Barbas and Pandya1989; for reviews, see Devinsky et al. Reference Devinsky, Morrell and Vogt1995; Paus Reference Paus2001). These anatomical connections can explain why the aMCC is part of an intrinsic brain network that shows increased activity when stimuli in the environment are personally salient (Seeley et al. Reference Seeley, Menon, Schatzberg, Keller, Glover, Kenna, Reiss and Greicius2007). They also explain why the aMCC is responsible for resolving action selection during situations involving conflicting sensory information (e.g., Grinband et al. Reference Grinband, Savitsky, Wager, Teichert, Ferrera and Hirsch2011; Milham et al. Reference Milham, Banich, Webb, Barad, Cohen, Wszalek and Kramer2001; Nelson et al. Reference Nelson, Reuter-Lorenz, Sylvester, Jonides and Smith2003; see Banich Reference Banich2009; Shackman et al. Reference Shackman, Salomons, Slagter, Fox, Winter and Davidson2011; van Snellenberg & Wager 2009). By extension, as a visceromotor (i.e., autonomic) control area sACC/pACC might be involved in resolving which sensory inputs influence the body when there are multiple sources of sensory input that can influence an organism's body state.

Our meta-analytic evidence is inconsistent with the locationist account that the ACC is the brain basis of sadness, but more consistent with a psychological constructionist hypothesis of ACC function. As compared to voxels within other brain regions, voxels within the sACC, pACC and aMCC did not have more consistent increases when participants were experiencing or perceiving instances of sadness than during any other emotion category (Fig. 6). As compared to voxels within other brain regions, a greater spatial extent of voxels within the aMCC had consistent increases in activation during instances of fear perception than the perception of any other emotion category (Table 1). The amygdala, which responds to motivationally salient exteroceptive sensory stimuli (see sect. 5.1 “The amygdala”), projects to this area of aMCC (Vogt & Pandya 1987), so it is possible that increased activity here reflects response preparation to salient stimuli in the environment.

Our logistic regressions revealed that increases in sACC were likely when participants were engaged in cognitive load (Fig. 5; Table S6). Cognitive load typically occurred in studies where participants were asked to attend to core affective feelings (e.g., focus on their feelings, rate their feelings) or affective stimuli (e.g., focus on an affective stimulus, rate a stimulus' emotional value) and so it is possible that this finding is indicative of the sACC's role in instantiating core affective feelings. Increased activity in the sACC was marginally (p < 0.09) likely when participants were evaluating their feelings, again consistent with this area's role as a visceromotor regulation site. Finally, consistent with a response selection hypothesis of aMCC function, increased activity in the aMCC was likely when participants were engaged in cognitive load (Fig. 5; Table S6).

5.5. Dorsomedial prefrontal cortex, medial temporal lobe, and retrosplenial cortex/posterior cingulate cortex

Our psychological constructionist approach hypothesizes that a range of other brain regions are important to realizing instances of emotion experience and perception, including dorsomedial prefrontal cortex (DMPFC), ventromedial prefrontal cortex (VMPFC), medial temporal lobe (MTL), and retrosplenial cortex/posterior cingulate cortex (PCC) (Fig. 2, panel B, purples), which are associated with the psychological operation of conceptualization. As part of the process of making meaning out of sensory cues, we hypothesize that these brain areas use stored representations of prior experiences to make meaning of core affective inputs that come from the self or observing others. Locationist views do not hypothesize specific roles for these brain regions in emotion because they are usually considered to have a “cognitive” function, insofar that they support memory (Vincent et al. Reference Vincent, Snyder, Fox, Shannon, Andrews, Raichle and Buckner2006), object perception (Bar 2009), and theory of mind (Mitchell Reference Mitchell2009). In our view, these brain regions should not necessarily be more involved in instances of one category of emotion than another, although we would expect them to be part of the more general neural reference space for discrete emotion.

As we predicted, our meta-analytic results revealed that regions of the conceptualization network such as DMPFC, MTL, and retrosplenial cortex (Buckner et al. Reference Buckner, Andrews-Hanna and Schacter2008) were part of the neural reference space for discrete emotion (Fig. 4).Footnote ⁸ Our findings indicate that the conceptualization network is integral in the experience and perception of discrete emotions, and are consistent with the hypothesis (in Barrett Reference Barrett2006b; Reference Barrett2009a; Reference Barrett2009b) that prior episodic experience helps shape experienced or perceived affect into meaningful instances of emotion.

Despite general involvement in emotion (Fig. 1; Fig. S3), there was some functional selectivity for instances of certain emotion categories in hubs within the conceptualization network. For instance, across our density analyses and logistic regressions, we found that instances of the experience of sadness (Tables 1 & 2) and experience of happiness (Table 1) were each associated with relatively greater consistent increases in activation in areas of DMPFC than other emotion categories. Consistent with the role of conceptualization in simulating episodic experience (Schacter et al. Reference Schacter, Addis and Buckner2007), our logistic regressions revealed that increased activity in DMPFC was likely when participants were engaging in emotion inductions involving recall and films (Fig. 5). Increased activity in some clusters of DMPFC was likely when participants were perceiving emotion in faces, bodies or voices. This finding is consistent with the psychological constructionist hypothesis that the conceptualization network is brought to bear when affective facial behaviors are perceived as emotional. Other clusters of DMPFC showed an opposite pattern: When participants were perceiving emotion, increased activity in DMPFC was not likely (Table S6). Just as perception of others and self-referential thinking involve overlapping yet distinct aspects of DMPFC (Ochsner et al. Reference Ochsner, Knierim, Ludlow, Hanelin, Ramachandran and Mackey2004a), some aspects of DMPFC might be functionally selective for conceptualization during emotion perception whereas others support conceptualization during emotion experience.

Several emotion categories were also associated with consistent increases in activation in the MTL (Tables 1 & 2; see Table S6). Our logistic regressions revealed that, as in the DMPFC, increased activity in the right hippocampus was likely to occur when participants perceived any instance of emotion in a face, body, or voice. Increased activity in the left hippocampus, on the other hand, was likely to occur when participants perceived instances of fear (Table S6). This finding is more likely to be related to the encoding of salient stimuli in memory than simulating prior experiences, as the amygdala also had increased activity during instances of fear perception and is known to have functional connectivity with the hippocampus during encoding of salient stimuli (Kensinger & Corkin Reference Kensinger and Corkin2004).

5.6. Anterior temporal lobe and ventrolateral prefrontal cortex

According to a psychological constructionist account, networks supporting language (e.g., Vigneau et al. Reference Vigneau, Beaucousin, Hervé, Duffau, Crivello, Houdé, Mazoyer and Tzourio-Mazoyer2006) should consistently show increased activity during instances of emotion experience and perception as linguistically-grounded concepts are brought to bear to make meaning of core affective feelings. In locationist accounts, language is thought to be epiphenomenal to discrete emotion (Ekman & Cordaro Reference Ekman and Cordaro2011), although recent behavioral studies show that categorical perception of discrete emotion is supported by language (Fugate et al. Reference Fugate, Gouzoules and Barrett2010; Roberson & Davidoff Reference Roberson and Davidoff2000; Roberson et al. Reference Roberson, Damjanovic and Pilling2007).

Consistent with the psychological constructionist view, nodes within networks supporting language were part of the neural reference space for discrete emotion (Fig. 4) In particular, the anterior temporal lobe (ATL) and ventrolateral prefrontal cortex (VLPFC) (Fig. 2, Panels A, B, C, green) had consistent increases in activity across studies of discrete emotion. The ATL supports language as a heteromodal association area involved in the representation of concepts (Lambon Ralph et al. Reference Lambon Ralph, Pobric and Jefferies2009; Pobric et al. Reference Pobric, Jefferies and Ralph2007; Rogers et al. Reference Rogers, Lambon Ralph, Garrard, Bozeat, McClelland, Hodges and Patterson2004) and the right ATL has been implicated in the representation of abstract social concepts (e.g., Zahn et al. Reference Zahn, Moll, Paiva, Garrido, Krueger, Huey and Grafman2009). Patients with semantic dementia have focal atrophy to the ATL, difficulty utilizing semantic knowledge, and exhibit deficits in emotion perception (Rosen et al. Reference Rosen, Pace-Savitsky, Perry, Kramer, Miller and Levenson2004) and empathy (Rankin et al. Reference Rankin, Gorno-Tempini, Allison, Stanley, Glenn, Weiner and Miller2006). Areas of the VLPFC, on the other hand, are implicated in semantic processing tasks (e.g., Gitelman et al. Reference Gitelman, Nobre, Sonty, Parrish and Mesulam2005), categorization of objects (e.g., Freedman et al. Reference Freedman, Riesenhuber, Poggio and Miller2001), representation of feature-based information for abstract categories (e.g., Freedman et al. Reference Freedman, Riesenhuber, Poggio and Miller2002; see Miller et al. Reference Miller, Freedman and Wallis2002), selection amongst competing response representations (e.g., Badre & Wagner Reference Badre and Wagner2007; Schnur et al. Reference Schnur, Schwartz, Kimberg, Hirshorn, Coslett and Thompson-Schill2009), and inhibition of responses (Aaron et al. Reference Aron, Robbins and Poldrack2004). It is therefore not clear that the VLPFC's role is functionally specific to language, but it is certainly functionally selective for language in certain instances. The VLPFC also helps comprise the ventral frontoparietal network that is thought to be involved in directing attention to salient stimuli in the environment (Corbetta & Shulman Reference Corbetta and Shulman2002; Corbetta et al. Reference Corbetta, Patel and Shulman2008), suggesting a more general role for this region in executive attention.

As compared to other brain regions, voxels within the ATL did not have more consistent increases during instances of one emotion category than others (Fig. S3). Our logistic regressions suggested that increased activity in the left ATL was more likely when participants were experiencing an instance of anger than any other emotion category, however (Fig. 5; Table S6). Instances of anger experience thus involve areas throughout the left frontal and temporal lobes (see sect. 5.2, “The anterior insula,” sect. 5.3, “The orbitofrontal cortex,” and sect. 5.7, “Dorsolateral prefrontal cortex”). Increased activity in the right ATL, on the other hand, was likely when participants were evaluating a stimulus (i.e., determining the emotional meaning of a face, voice, or picture; Table S6). This finding is consistent with the hypothesis that language is brought to bear when constructing emotional percepts from exteroceptive sensations.

Our density analyses revealed that as compared to voxels within other brain regions, voxels within the right VLPFC had more consistent increases during instances of disgust perception than during the perception of any other emotion category; these findings were confirmed with a logistic regression (Table 1; Table S6). χFootnote ² analyses revealed that a subset of the voxels identified in the density analysis were functionally selective for instances of disgust perception (Table 2), although they were not specific to instances of disgust (Fig. S3). The most common finding across our logistic regressions linked increases in the left VLPFC to instances in which participants were explicitly paying attention to emotional information (Fig. 5; Table S6). As in other left frontal and temporal areas (see sects. 5.2, “The anterior insula,” 5.3, “The orbitofrontal cortex,” 5.6, “Anterior temporal lobe and ventrolateral prefrontal cortex”), increased activity in the left VLPFC was likely when participants were experiencing or perceiving instances of anger.

5.7. Dorsolateral prefrontal cortex

According to a psychological constructionist account, networks supporting executive attention (see Miller & Cohen Reference Miller and Cohen2001; Petrides Reference Petrides2005; for a meta-analysis, see Wager & Smith Reference Wager and Smith2003) should consistently show increased activity during instances of emotion experience and perception because executive attention directs other psychological operations during the construction of emotion. Locationist accounts do not propose specific roles for these networks in emotion, although they might allow that networks supporting executive attention take part in regulation of emotion after it is generated (as in Ochsner et al. Reference Ochsner, Ray, Cooper, Robertson, Chopra, Gabrieli and Gross2004b; Urry et al. Reference Urry, van Reekum, Johnstone, Kalin, Thurow, Schaefer, Jackson, Frye, Greischar, Alexander and Davidson2006).Footnote ⁹

Consistent with our psychological constructionist hypothesis, nodes within networks supporting executive attention were part of the neural reference space for discrete emotion. In particular, the VLPFC and dorsolateral prefrontal cortex (DLPFC) (Fig. 2, Panel A, orange and striped green/orange) had consistent increases in activity across studies of discrete emotion. The DLPFC is part of the dorsal frontoparietal network that is thought to be involved in top-down, goal-directed selection for responses (Corbetta & Shulman Reference Corbetta and Shulman2002; Corbetta et al. Reference Corbetta, Patel and Shulman2008). Consistent with this functional connectivity, bilateral DLPFC is known to be involved in working memory (e.g., Champod & Petrides Reference Champod and Petrides2007; Constantinidis et al. Reference Constantinidis, Williams and Goldman-Rakic2002) and in the goal-directed control of attention (e.g., Rainer et al. 1998; see Miller Reference Miller2000).

We predicted that DLPFC would be part of the neural reference space for emotion (Fig. 4) because these voxels would be active during mental states in which participants attended to emotional feelings or perceptions (i.e., when participants had to hold affective information in mind in order to categorize it). Consistent with this prediction, increased activity in the right DLPFC was likely when participants were explicitly evaluating stimuli (Fig. 5; Table S6). Our density analyses also revealed that as compared to voxels within other brain regions, voxels in the right DLPFC were more likely to have increased activity during instances of anger perception than any other emotion categories (Table 1). Our χFootnote ² analyses indicated that some of these voxels were functionally selective to perceiving instances of anger (Table 2), although they were not specific to perceiving instances of anger (Fig. S3).

5.8. The periaqueducal gray

The periaqueducal gray (PAG) is involved in regulating the autonomic substrates that allow for behavioral adaptations such as freezing, fleeing, vocalization, and reproductive behavior (e.g., Carrive et al. Reference Carrive, Bandler and Dampney1989; Behbehani Reference Behbehani1995; Gregg & Siegel Reference Gregg and Siegel2001; Kim et al. Reference Kim, Rison and Fanselow1993; Lovick Reference Lovick1992; Mobbs et al. Reference Mobbs, Petrovic, Marchant, Hassabis, Weiskopf, Seymour, Dolan and Frith2007; Van der Horst & Holstege Reference Van der Horst and Holstege1998) and also sends projections back to cortical sites involved in the regulation of visceral activations in the body (An et al. Reference An, Bandler, Ongur and Price1998; Mantyh Reference Mantyh1983). It is believed that certain adaptations are associated with certain emotion categories (e.g., animals freeze in fear, aggress in anger) but such links are far from empirically clear. Humans (like other mammals) do many things during instances of anger, for example. Sometimes humans yell, sometimes they hit, sometimes they remain very still, and sometimes they smile. Even rats do many things within a single emotion category: In the face of a threat, rats can freeze (e.g., LeDoux et al. Reference LeDoux, Ciccetti, Xagoraris and Romanski1990), flee (Vazdarjanova & McGaugh Reference Vazdarjanova and McGaugh1998), or engage in “defensive treading,” where they kick bedding in the direction of a known threat (Reynolds & Berridge Reference Reynolds and Berridge2002; Reference Reynolds and Berridge2003; Reference Reynolds and Berridge2008). In all these instances, PAG activity and the associated autonomic states it produces, are yoked to the action, and not to the emotion category. As a result, a psychological constructionist approach views PAG activity as nonspecifically involved in instances of emotion. A locationist approach has linked the PAG to distinct circuits corresponding to several emotion categories: rage, fear, joy, distress, love and lust (Panksepp Reference Panksepp1998). In a psychological construction approach, the assumption is that a given dedicated circuit for a specific behavioral adaptation (e.g., withdrawal) will be active across a range of emotion categories (e.g., a person can withdraw in instances of both fear and anger), and different dedicated circuits within the PAG (e.g., fight, flight) will be active within instances of a single emotion category depending upon which behavioral adaptation is more relevant for the immediate context.

Testing any hypothesis about the specificity of a subcortical region like the PAG is practically impossible, given the spatial and temporal limitations of brain imaging. Still, it is instructive to note that the PAG was consistently activated within the neural reference space for discrete emotion (even though subjects were lying still and not engaging in any overt physical action; see Fig. S4 in the supplementary materials, available at http://www.journals.cambridge.org/bbs2012008). Moreover, we did not find evidence of functional specificity for the PAG in our meta-analysis. It is possible that given the resolution problems, different circuits within the PAG were specifically active for discrete emotions. That said, it is also entirely plausible from the behavioral data that humans, like animals, perform a range of actions within a single category, and perform the same action at times across categories (even if it does not match our stereotypes of emotion–action links). In this meta-analysis, increased activity in the PAG did not correspond to any particular emotion category more than another (although instances of the experience of sadness were associated with consistent increases in activation in one voxel within ventral PAG; Tables 1 & 2). The logistic regressions demonstrated that increased activity in the PAG was likely when participants were experiencing or perceiving an instance of any high-arousal emotion category (Table S6). Consistent with this finding, activity in a separate cluster of PAG was likely when participants were experiencing instances of fear (Table S6). In a previous meta-analysis, we found that the PAG was most likely to have increased activity during unpleasant emotions (Wager et al. Reference Wager, Barrett, Bliss-Moreau, Lindquist, Duncan, Kober, Joseph, Davidson and Mize2008). Since all high-arousal emotion categories in our database were unpleasant (e.g., fear, anger, disgust), our present findings are consistent with Wager et al. (Reference Wager, Barrett, Bliss-Moreau, Lindquist, Duncan, Kober, Joseph, Davidson and Mize2008). Future research should probe whether the PAG preferentially shows increased activity during unpleasant states, highly aroused states, or during states that are both unpleasant and highly aroused.

5.9. Visual cortex

From our psychological construction approach, we would not be surprised to observe that voxels within visual cortex (or any sensory modality) show increased activation during emotion. In its most basic form, our hypothesis is that emotion emerges as a situated conceptualization of internal sensations from the body and external sensations from the world to create a unified conscious experience of the self in context. In fact, regions of visual cortex were some of the most frequent to appear in our meta-analytic findings (replicating several recent meta-analyses; e.g., Fusar-Poli et al. Reference Fusar-Poli, Placentino, Carletti, Landi, Allen, Surguladze, Benedetti, Abbamonte, Gasparotti, Barale, Perez, McGuire and Politi2009; Kober et al. Reference Kober, Barrett, Joseph, Bliss-Moreau, Lindquist and Wager2008; Vytal & Hamann Reference Vytal and Hamann2010). It is beyond the scope of this article to discuss these findings in detail, but we found that instances of fear experience, anger perception, and disgust experience were consistently associated with increased activity in regions of visual cortex ranging from V2 to visual association cortex (Tables 1 & 2). Our logistic regressions revealed that activation in visual cortex was not merely a by-product of the methods used. Although increased activity in visual cortex was likely when visual methods were used (e.g., pictures, faces, studies of perception; see Table S6), it was also likely in studies of unpleasant, high-arousal emotions (e.g., fear, disgust, unpleasant emotions more generally; Table S6). Together, these findings indicate that experiences or perceptions of unpleasant emotion categories are realized by brain states that include increased activity in visual cortex. See Gendron et al. (in preparation) for a discussion.