The results support our preliminary hypothesis that a situated conceptualization draws on neural systems that process relevant information. In the discussion that follows, we review extensive supporting evidence for this hypothesis. The results further support the two critical hypotheses that follow from the preliminary hypothesis. First, as Conceptual Act Theory predicts, different situated conceptualizations represented the same emotion in different situations. Inconsistent with basic emotion theories, constant relatively unique modules did not represent the same emotion across different situations. Second, situated conceptualizations were composed of information that represents concepts, situations, and their interaction, drawn from a common neural circuitry distributed throughout the brain. The following two sections examine the implications of our results for each hypothesis in turn, while simultaneously addressing the preliminary hypothesis.
Situated Conceptualizations for Emotion Concepts
The results in , , and offer strong support for Hypothesis 1 that an emotion is constructed differently depending on the situation. As and show, anger and fear were represented differently when experienced in a physical danger vs. a social evaluation situation. Although some brain areas were common across both situation types for the same emotion, many other brain areas were only active in one situation type or the other. Furthermore, the overall percentage of voxels unique for an emotion concept in a particular situation was typically large, ranging from 27% to 53% across situated conceptualizations for the emotion concepts (). Thus, the situation in which an emotion concept was experienced shaped how the emotion was instantiated in the brain. We next present a brief overview of the shared and unique activations observed in the situated conceptualizations for each emotion concept. The brain regions and general functions summarized in this overview receive more detailed treatment in later sections. Thus, we do not integrate these initial summaries with previous literature here, but do so in the next section when addressing the neural circuitry associated with Hypothesis 2.
Situated conceptualizations of anger
Approximately two-thirds of the voxels in the situated conceptualizations for anger were shared across the two situations, originating in concept main effects and interactions ( and ). Lateral and medial orbitofrontal cortex, dorsal anterior cingulate, medial prefrontal cortex, the temporal poles, supplementary motor area, right middle temporal gyrus, left inferior frontal gyrus, and bilateral posterior superior temporal gyrus were active in both situated conceptualizations. Based on this activation profile, we suggest that representations of anger in both situations involved facets of socio-emotional processing, including integration of internal and external sensory states (lateral orbitofrontal cortex), visceromotor control (medial orbitofrontal cortex), mentalizing (medial prefrontal cortex), action planning (supplementary motor area), and language (inferior frontal gyrus, middle and superior temporal gyrus).
Numerous situationally unique activations were also observed in the situated conceptualizations for anger, originating in situation main effects and interactions. Approximately one-third of the active voxels occurred in only one of the situations ( and ). In physical danger situations, anger was directed towards the self because one had acted carelessly. Bilateral posterior insula, bilateral superior temporal gyrus, bilateral parahippocampal gyrus, mid-cingulate gyrus, and left dorsolateral prefrontal cortex were more active during anger in this context. We propose that these activations reflect cognitive control and inner speech (dorolateral prefrontal cortex, superior temporal gyrus), as well as interoceptive processing (insula) and orienting of the body (mid-cingulate, parahippocampal cortex), relevant to experiencing anger directed inward towards oneself. In social evaluation situations, anger was directed towards an unfair other. Ventromedial prefrontal cortex, bilateral inferior parietal cortex, and posterior occipital regions were more active during anger in this context. We propose that these activations reflect the evaluation of oneself and others (ventromedial prefrontal cortex), as well as the visualizing of details (occipital) and assessing extra-personal space for action (inferior parietal cortex), specific to experiencing anger directed outward towards another.
Situated conceptualizations of fear
Similar to anger, situated conceptualizations of fear across the physical danger and social evaluation situation types shared common processing areas, originating exclusively in concept main effects. Notably, however, the extent of these common processing areas was lower than for any other concept, given that only about half of the voxels were shared across situations ( and ). The shared activations for fear included a subset of the regions observed for anger. Specifically, lateral and medial orbitofrontal cortex, dorsal anterior cingulate, medial prefrontal cortex, supplementary motor area, and the temporal poles were active in both situated conceptualizations for fear. Like anger, the situated conceptualizations for fear in both situations included facets of socio-emotional processing. Unlike anger, however, shared activations for fear did not involve brain regions typically involved in auditory processing and language (e.g., left inferior frontal gyrus, bilateral superior temporal gyrus), suggesting that spoken language was more central for anger.
Fear exhibited considerable specificity to the situation, given that approximately half of the active voxels were situationally unique. Again, activations unique to one situation originated in situation main effects and interactions. In physical danger situations, the fear experienced was related to bodily harm. Mid-cingulate, as well as bilateral posterior insula, parahippocampal cortex, inferior parietal cortex, and superior temporal gyrus were more active during fear in this context. This profile of activation was the most sensory-motor oriented of the situated conceptualizations for the emotion concepts. We propose that these activations reflect action planning in the visuo-spatial environment (inferior parietal cortex, parahippocampal cortex), and also the interoceptive (insula) and auditory (superior temporal gyrus) processing specific to experiencing fear of physical harm. In social evaluation situations, the fear experienced was related to being judged negatively by another. Specifically, ventromedial prefrontal cortex, left posterior orbitofrontal cortex, left inferior frontal gyrus, left dorsolateral prefrontal cortex, left temporal pole, and posterior occipital cortex were more active during fear in this context. We propose that these activations reflect the evaluation of oneself and others (orbitofrontal cortex, ventromedial prefrontal cortex), access of social knowledge about individuals (temporal pole), cognitive control (dorsolateral prefrontal cortex; inferior frontal gyrus), and visualizing details (posterior occipital) specific to experiencing fear of social judgment (instead of physical harm).
Anger vs. fear
Judging by , , and , one might be tempted to conclude that anger generally exibits less variability across situations than does fear. An important possibility, however, is that the situational elements that were manipulated in the two situation types were stronger for fear (bodily harm vs. social evaluation) than for anger (directed towards self vs. directed towards another). Future research is required to distinguish these possibilities. We strongly suspect that the magnitude of situation effects is likely to vary widely depending on the particular situation manipulations implemented.
Implications for theories of basic emotion
According to basic emotion theories, emotions are natural kinds, each produced by a unique circuit stable across instances of the emotion (Ekman, 2003
; Izard, 2007
; Panksepp, 2000
). From this perspective, an emotion such as fear
should activate one or more brain regions significantly more than should any other emotion, and should also show stability in the areas activated across its instances. Clearly, our results did not display consistency within instances, as shown by the different activation patterns for the two situated conceptualizations of each emotion (, ).
To examine whether one or more regions were activated significantly more during anger or fear than for all other concepts, we further examined the concept main effects. Whenever one concept (across both situation types) was more active than the other three concepts (across both situation types) in a cluster, a large bolded + exists for that concept in the concept main effects table (). As can be seen, observe showed the most selective pattern of neural activity according to this criterion, followed by plan and then anger. To rule out the possibility that only one of the situation-concept conditions reflected the “true” basic emotion (e.g., fear during physical danger), we also looked for this profile of activation in the interaction effects. No single situation-concept condition (e.g., physical-fear) was ever significantly more active than all other conditions in an interaction cluster.
The experience of fear
in our study did not selectively activate any region more than the other three concepts. Because our paradigm oriented participants towards experiencing fear
(not towards detecting it in ambiguous contexts), our findings are consistent with meta-analyses that distinguish emotion perception from emotion experience. Whereas the perception of fear
(along with other emotions) consistently activates the amygdala, the experience of fear
does not (Lindquist et al., 2010
; Wager et al., 2008
). Although other meta-analyses have found the amygdala to be consistently (but not specifically) active for fear
, these analyses did not distinguish between perception vs. experience (Murphy et al., 2003
; Phan et al., 2002
; Vytal & Hamann, in press
). Recent evidence further indicates that the amygdala is not selective for fear
per se, but that it responds to motivationally salient events that require attention and learning (Barrett, 2009a
; Whalen et al., 2009
; Winston, O’Doherty, & Dolan, 2003
; Winston et al., 2005
Medial orbitofrontal cortex was more active during anger
than during all other concepts. Importantly, though, fear
showed more activity in this region than observe
, but less activity than anger
. Thus, anger
did not selectively activate this region in an absolute manner, given that it was also active during fear
, but to a lesser degree. Furthermore, the orbitofrontal cluster we observed is more medial than those reported for anger
in recent meta-analyses (Murphy et al., 2003
; Vytal & Hamann, in press
; but see Lindquist et al., 2010
). In contrast to lateral orbitofrontal cortex, medial areas are highly connected with visceromotor structures in the hypothalamus and brainstem (Ongur & Price, 2000
). Thus, the medial activation observed here suggests that anger
was associated with viceromotor processing, more so than the other concepts. It is clear, however, that activity in this region constituted only one part of a distributed set of processing areas for anger
in a particular situation—there was much more to anger
than this specific process. And again, this region was more active during fear
than during observe
, demonstrating that anger
is not completely selective in utilizing its processing resources.
To summarize, the lack of selective responses for anger and fear is consistent with our conclusion that situated conceptualizations represented these emotions. Constant, relatively unique circuits did not represent the same emotion in different situations, as basic emotion theories predict.
The Composition of Situated Conceptualizations for Emotion
According to Hypothesis 2, the composition of a situated conceptualization should reflect contributions from different compositional elements in shared neural circuitry for emotion distributed across the brain. As , , , and illustrate, the representation of an emotion in a given situation was composed of information from emotion concepts (concept main effects), the situations in which emotions were experienced (situation main effects), information common to emotion concepts and related situations (overlapping concept and situation main effects), and information specific to experiencing an emotion concept in a specific situation (interaction effects). These compositional elements of emotion representation combined to form the situated conceptualizations in and (summarized in ).
In the following sub-sections, we first explore each compositional element that contributed to the representation of situated conceptualizations. We then address the related prediction that these compositional elements are generally drawn from shared neural circuitry distributed throughout the brain that produces situated conceptualizations of emotions dynamically. illustrates each effect type from the factorial ANOVA in a different color, and illustrates the close proximity of different effect types to one another in various brain regions.
Whole-brain activations for each effect type displayed on an inflated surface. The inflated surface is only used for display purposes; analyses were not computed in this space. L is left and R is right.
Contributions from concepts (concept main effects)
As and specify, and as and illustrate for concept main effects, information from concepts contributed significantly to the composition of situated conceptualizations for emotion. Specifically, certain information was active for the same emotion in different situations, suggesting that it was drawn from conceptual knowledge about the emotion common across situations.
As proposed earlier, we do not assume that emotions have conceptual cores. Instead, we assume that emotion concepts, like other concepts, are dynamical systems whose collections of situated conceptualizations and partial abstractions change constantly over time, producing representations that vary widely across situations (e.g., Barsalou, 1987
). From this perspective, any information active for an emotion across both situations simply reflects conceptual information that happened to be relevant in both situations.
Notably, many brain regions active during experiences of fear
were also active during experiences of anger
, and also plan
. Regions in medial prefrontal cortex played a primary role in contributing information across situations to all three concepts, along with regions of medial orbitofrontal cortex and dorsal anterior cingulate. These regions are generally associated with emotion perception, emotion experience, mentalizing, attitudes, evaluation, self-concepts, and understanding the minds of others (for reviews see Amodio & Frith, 2006
; Mitchell, 2009b
; Van Overwalle, 2009
). Medial prefrontal cortex has also been highlighted as a critical part of the “core” (Buckner & Carroll, 2007
) or “default” network (Gusnard & Raichle, 2001
), often hypothesized to be a global system for inner-oriented processing (Golland et al., 2008
), self-related processing (Buckner & Carroll, 2007
), contextual processing (Bar, 2004
), and processing that involves bringing prior experience to bear on constructing the present psychological moment (Barrett, 2009a
). The medial prefrontal activations extended up into the supplementary motor area, suggesting that planning internally generated action was also central to anger
, and plan
(Nachev, Kennard, & Husain, 2008
; Picard & Strick, 1996
). Left lateral orbitofrontal cortex and the temporal poles also showed a similar profile, active across these three concepts. Increasing evidence indicates that lateral orbitofrontal cortex integrates external and internal sensory information (Ongur & Price, 2000
), and is sensitive to the affective properties of stimuli (Kringelback & Rolls, 2004
; Wager et al., 2008
). Increasing evidence suggests that the temporal poles represents individuals in social contexts (Damasio et al., 2004
; Drane et al., 2008
; Simmons & Martin, 2009
; Tranel, 2006
Notably, however, the large majority of activations for the concept main effects occurred in posterior sensory-motor regions for the two non-affective abstract concepts, observe
. Consistent with our proposal that distributed patterns of activity across relevant modalities represent concepts, visual, auditory, and motor areas were all activated more active for these concepts than for the emotion concepts. Because visual, auditory, and motor processing are all central to observing the world and planning action in it, the activation of relevant neural systems for representing observe
is not surprising. Additionally, clusters in bilateral posterior insula were also more active for observe
than for the emotion concepts, suggesting that interoception was especially important for observing and planning (Craig, 2002
). Although this might seem surprising, we will see that an adjacent cluster in posterior insula was active for the emotion concepts as well, but only in physical danger situations (present in an interaction effect).
As predicted, the profiles of stable activations across situations during fear and anger reflected processes associated with mentalizing, such as internally evaluating the current situation, projecting future outcomes, accessing person knowledge, and planning actions. This pattern contrasted with very different predicted profiles across situations for observe and plan. For observe, neural systems became active that perform externally-oriented visual, auditory, motor, and spatial processing, as well as internally-oriented interoception associated with monitoring. For plan, these posterior perceptual regions were again active, together with medial prefrontal areas associated with mentalizing, suggesting that planning requires integrating or shifting between mentalizing and operating in the environment.
Contributions from situations (situation main effects)
As and specify, and as and illustrate, representations of situations contributed significantly to the composition of situated conceptualizations for emotion. Specifically, certain information was active for the same situation across different concepts, suggesting that it was drawn from conceptual knowledge about the situation. As a situated conceptualization became active to represent an emotion in a particular situation, it drew on knowledge about the situation, as well as on knowledge about the emotion. These two types of compositional elements were then integrated to represent the emotion in a situated manner, along with information found for joint main effects and interaction effects.
When the concepts were experienced in physical danger situations, mid-cingulate and bilateral parahipocampal gyrus were significantly more active than during social evaluation situations. Much evidence suggests that mid-cingulate integrates evaluation of the present situation with skeletomotor control and orientation (Rolls, 2005
), and further implicates this region in nociception (Vogt, 2005
; Vogt, Berger, & Derbyshire, 2003
). In contrast to anterior cingulate, mid-cingulate cortex contains motor areas that project to the motor cortices and that play roles in response selection (Morecraft & Van Hoesen, 1992
; Vogt, 2005
). This main effect suggests that orienting and/or controlling movement in response to physical discomfort is relevant to experiencing fear
, and plan
in physical danger situations. Bilateral parahippocampal gyrus was also active during these situations, suggesting that large-scale visuo-spatial settings were being simulated (Bar, 2004
; Epstein, 2005
). Taken together, these mid-cingulate and parahippocampal activations suggest that orienting the body in a large-scale visuo-spatial scene was a common element in physical danger situations across concepts, consistent with our initial predictions.
Following social evaluation situations, ventromedial prefrontal cortex was significantly more active across concepts than following physical harm situations. This region is often associated with monitoring the value of possible outcomes (Amodio & Frith, 2006
), self-referential processing (Mitchell, Heatherton, & Macrae, 2002
; Northoff et al., 2006
), and visceromotor control (Ongur & Price, 2000
). A posterior occipital cluster (BA 17/18) was also active following social evaluation situations. Activation in early occiptial regions during visual imagery has been observed when tasks involve high-resolution details and shapes rather than spatial orientation (Kosslyn & Thompson, 2003
), suggesting that the processing of visual detail was important, perhaps for faces. As predicted, social evaluation situations involved self-related, evaluative processing instead of pressing bodily concerns, as for physical harm situations. Interestingly, social evaluation situations also recruited the processing of fine-grained visual details instead of large-scale visuo-spatial scenes.
Because the regions for the situation main effects were active across all four concepts, one might assume that they were peripheral to each concept’s representation. We propose, however, that these effects were just as central to representing each concept as were the other effect types. For example, representing visuo-spatial scenes and responses to pain are both central for experiencing fear in physical danger situations. Analogously, representing psychological attributes of oneself and the facial detail of others are central for experiencing fear in social evaluation situations. Without the presence of this critical information in the respective situation, it does not seem possible to experience the relevant form of fear.
Overlapping contributions from concepts and situations (both main effects)
As and specify, and as and illustrate, some information used to compose situated conceptualizations for emotions existed both in an emotion concept and in situation knowledge. In these cases, information typically relevant for a concept across situations was also often relevant in a particular type of situation across concepts. Such activations further indicate that concepts are situated, given this situational information in their representation. Interestingly, however, some situated information in a concept appears to be broadly represented across many concepts.
A region in dorsomedial prefrontal cortex was active during all concepts in social evaluation situations, and also active during anger, fear, and plan. One interpretation is that this cluster reflected the importance of person knowledge and theory of mind across all four concepts in social situations relative to physical situations, but more so for anger, fear, and plan than for observe. A very different profile occurred for a region in superior temporal gyrus, being more active for physical situations than for social situations, and being more active for plan and observe than for anger and fear. This pattern may reflect the importance of auditory processing across all four concepts in physical situations, but more so during plan and observe, which generally involved more external sensory processing.
Contributions from concept-situation interactions (interaction effects)
As and specify, and as and illustrate, many neural activations were specific to experiencing an emotion concept in specific situations. One possibility is that these activations reflect information stored in a concept that only becomes active in particular situations, not all (e.g., Barsalou, 1982
). Another possibility is that these activations reflect information constructed on-line to integrate a concept into a situation, with this information later being stored with the concept (e.g., Barsalou, 1983
). We suspect that both mechanisms could underlie the interaction effects observed here (e.g., Barsalou, 1987
Interestingly, instead of one or two dominant patterns emerging as for the main effects, these clusters exhibited many unique patterns of activation across conditions. All clusters but one (precuneus) contained at least one significantly active emotion condition. Thus, it was not the case that the non-emotion concepts drove the interaction effects, as basic emotion theories might predict. Instead, the emotion concepts exhibited strong variability across situation types. For detailed discussion of these interaction effects and their relations to relevant literature, see the Supplemental Materials
. Here we summarize that discussion. It is important to note that we did not attempt to generate detailed predictions about interaction effects initially. Thus, our interpretations of the interaction effects are informed by other findings in the literature.
Interaction clusters were located primarily in lateral prefrontal, temporal, parietal, and insular cortices. A cluster in left lateral orbotifrontal cortex was active for fear in social situations and for anger in both situations, suggesting that fear in physical situations, relative to the other emotion conditions, may have involved less attention to subjective feelings of unpleasantness, perhaps because attention was focused more on actions taken to avoid a physical threat. Clusters in bilateral posterior insula were active for fear and anger in physical but not social situations, suggesting that the monitoring of interoceptive states was especially important when physical harm was anticipated. Clusters in left dorsolateral prefrontal cortex and inferior frontal gyrus were more active when fear was experienced in social situations than when fear was experienced in physical situations, suggesting that executive control was especially important for coping with threatening evaluations in social situations. Conversely, clusters in temporal auditory areas showed the opposite pattern, suggesting that monitoring environmental sounds and inner speech were especially important for coping with possible bodily harm in physical situations. Finally, bilateral inferior parietal cortex was active for fear in social situations but for anger in physical situations, suggesting that fear in physical situations involves acting on threats in the environment, whereas anger in social evaluation situations involves initiating retribution towards another person.
Constructing Emotion Instantiates Distributed Neural Circuitry
As described earlier, Hypothesis 2 predicts that the different compositional elements of situated conceptualizations should generally be drawn from common neural circuitry distributed throughout the brain that produces situated representations of emotions dynamically. In other words, certain brain regions should consistently play central roles in representing the same emotion in different situations, and in representing different emotions. The results reported here strongly confirm this prediction.
First, it is important to note that many of the brain regions observed are not, strictly speaking, functionally specific to emotion per se. These regions are also frequently involved in representing other abstract concepts—as illustrated by their roles in representing plan
. This pattern supports Conceptual Act Theory, which proposes that an instance of emotion (i.e., a situated conceptualization) is a compositional representation constructed from basic psychological components not specific to emotion (Barrett, 2009a b
; Gendron & Barrett, 2009
). Such findings are also broadly consistent with meta-analyses of the neuroimaging literature which show that brain regions typically referred to as “affective,” “cognitive, and “perceptual” are all consistently active during emotion (Lindquist et al., 2010
; Kober et al., 2008
; Pessoa, 2008
; Wager et al., 2008
In our results, we observed activations during fear
in five of the six functional networks established in the Kober et al. meta-analysis. Interestingly, many of the activations during plan
—our two non-emotion concepts—also occurred in regions that this meta-analysis identified (especially in temporal and occipital cortices). Because these concepts were embedded in emotional situations, it is perhaps not surprising that they activated brain regions reported in meta-analyses of emotion. As described above, though, it is likely that these processing areas enter into the processing of many concepts. Because this article focuses on emotion, however, our discussion only addresses these processing areas with respect to the emotion concepts. For detailed discussion of these processing areas and their connection to relevant literature, see the Supplemental Materials
. Here we summarize that discussion.
Three regions often central for emotion in the literature were also central in our experiment: medial prefrontal cortex, lateral prefrontal cortex, and insular cortex. As illustrates, multiple effect types from the factorial ANOVA lay adjacent to one another in these regions, reflecting functional heterogeneity in a given region.
Much of medial prefrontal cortex was active in either concept main effects, situation main effects, or in both main effects, including medial orbitofrontal cortex, ventromedial prefrontal cortex, dorso-medial prefrontal cortex, and supplemental motor area. Interestingly, these areas did not contain any interaction effects. Instead, these areas contained concept effects for anger, fear, and plan, along with situation effects for social situations, implicating the importance of social evaluation, self-referential processing, and action planning in these three concepts and in knowledge about social situations.
In lateral prefrontal cortex, a concept main effect in left orbitofrontal cortex adjoined an interaction effect in dorsal regions of left orbitofrontal cortex that extended up the inferior lateral surface. For the concept main effect, a left lateralized cluster in orbitofrontal cortex was more active for anger, fear, and plan than for observe across both situations. As suggested earlier, this cluster may reflect the general importance of evaluation and mentalizing for these three concepts. An adjoining interaction effect in lateral orbifrontal cortex was active for anger in both situations and for fear only in social situations. Additional interaction effects showing the same pattern as for fear occurred more dorsally in inferior frontral gyrus and lateral prefrontal cortex. One interpretation of all these interaction effects is that they reflect the importance of intereceptive information in controlling attention when processing individuals (other people for fear and anger in social evaluations situations, and oneself for anger in physical harm situations). Conversely, these areas do not become active for fear in physical harm situations, because responding rapidly to external physical threats is more important.
Finally, concept main effect and interaction clusters occurred adjacently to one another in posterior insula. In the concept effect cluster, insula activity during plan and observe was greater than during fear and anger. In the interaction cluster, insula activity was greater during plan and observe in both situations, and also during fear and anger in physical danger situations. A somewhat similar profile was observed in mid-cingulate, where adjacent clusters exhibited a concept main effect for plan and observe and a situation main effect for physical danger situations. One interpretation of these activations is that for observe and plan across situations, and for all concepts in physical situations, the insula represents salient interoceptive information that initiates motor processing in mid-cingulate.
In summary, different effect types lay adjacent to one another in three cortical regions central to emotion experience (medial prefrontal, lateral prefrontal, and insular cortices). These results further support the proposal that emotions instantiate distributed neural circuitry that composes situated conceptualizations dynamically. More speculatively, we propose that the different effect types represented in a common brain region may play slightly different roles in emotion experience, with the precise functions of these individual areas remaining to be established in future work.
Our results support the Conceptual Act Theory of Emotion. Consistent with this theory, different situated conceptualizations represent the same emotion concept in different situations. Furthermore, situated conceptualizations of emotion instantiate common neural circuity distributed across the brain that is not specific to emotion per se. Specific instances of emotion are constructed dynamically within this circuitry to represent an emotion in a particular situation.