Olsson On Social Cognition in Emotion
Olsson On Social Cognition in Emotion
Olsson On Social Cognition in Emotion
Cognitive-emotional interactions
Although recent research has shown that social Understanding emotions in self and others
cognition and emotion engage overlapping regions of The ability to understand both another person’s and one’s
the brain, few accounts of this overlap have been offered. own emotional states is essential for virtually all aspects of
What systems might be commonly or distinctively social behavior and crucially depends upon MSA. Indeed,
involved in each? The close functional relationship be- emotion understanding – by definition – requires a causal
tween social cognition and emotion might be under- attribution about the intentions behind an action. Evi-
stood in terms of a central role for mental state dence suggests that MSA contributes to emotion under-
attribution in the understanding, learning and regulation standing through the operation of both rapid stimulus-
of emotion. In each of these cases, mental state attribu- driven processes [4,5] and more deliberative, reflective and
tions might be supported by either stimulus-driven or conceptually driven processes [6–8].
more reflective processes. Evidence for the neural bases of stimulus-driven MSA
came initially from imaging studies showing that some
Exploring the role of mental state attribution in motor regions respond during both the execution and
emotion observation of specific movements [4]. The idea was that
Whether viewed from a phyologenetic or an ontogenetic if motor regions code the intentions behind one’s own
perspective, it is clear that the abilities to understand, action, then if activated when observing another person
learn from and behave appropriately towards one engaging in the same action, they could support a direct
another were as essential for our homonid ancestors experiential understanding of that person’s intention [4,9].
as they are for a developing child [1]. In the past decade, This ‘shared representation’ logic guided subsequent
insight into the neural mechanisms supporting these studies of the direct experience and observation of pain
abilities has been provided by two burgeoning fields of or emotion that also showed activation of overlapping
research: social cognitive neuroscience and affective neural systems, including most prominently the two cor-
neuroscience. Although these fields developed largely tical regions that receive ascending viscerosensory inputs:
independently [2], for multiple reasons the boundaries the anterior insula (AI) and the midportion of the anterior
between the phenomena they study are becoming cingulate cortex (mACC) [4,7,10–15]. The AI is believed to
increasingly blurred (Box 1). Perhaps chief among them support affective experience in part through interoceptive
is the finding that ostensibly different types of social awareness of these body state inputs [16,17], whereas the
cognitive or emotional abilities recruit similar suites of ACC is thought to code affective attributes of pain, such as
cortical and subcortical neural systems. Although this the perceived unpleasantness (as opposed to sensory-dis-
fact has been noted [3], to date few accounts of the criminative properties, such as location and intensity) [18–
apparent interdependence of social cognition and 20] and motivate appropriate behavior through projections
emotion have been advanced. to motor and autonomic centers [16,21]. The engagement of
Here, we review recent work suggesting that this the AI, ACC and other regions is thought to facilitate the
relationship can be understood – at least in part – in terms automatic sharing of – and hence direct experiential un-
of a fundamental role of one type of social cognitive derstanding of the intentions behind – affective states,
capacity in processing emotion: the ability to explain beha- which in turn might provide a substrate for empathic
vior in terms of intentional mental states, which we will connection [7,13].
refer to as mental state attribution (MSA; Box 2). The role Emotion understanding is not always so simple, how-
of MSA can be considered in three domains: (i) understand- ever, because nonverbal cues to emotion are often ambig-
ing emotion, (ii) learning emotionally significant infor- uous. In such cases, additional information is needed to
mation and (iii) regulation of emotional responses. For constrain attributions about a person’s intentions and
each domain, we discuss the roles in emotion processing hence their emotional state. One source of information is
of systems supporting MSAs that vary in their degree of our prior experience with that person and knowledge about
representational complexity and reflective control. Based antecedent events. For example, wide open eyes could
on this review, we propose a neural framework for un- mean that someone is either afraid or surprised – and
derstanding the role of social cognition in emotion that can elicit amygdala activity accordingly – depending on what
guide future research. one knows has just happened to them [22]. Similarly,
activation of shared representations – and presumably
Corresponding authors: Olsson, A. (aolsson@paradox.psych.columbia.edu);
empathic connection – might be blocked if one perceives
Ochsner, K.N. (kochsner@paradox.psych.columbia.edu). another to be a past or potential competitor [23,24].
1364-6613/$ – see front matter ß 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.tics.2007.11.010 65
Review Trends in Cognitive Sciences Vol.12 No.2
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and with the MPFC when observing others in pain when, and how, we use similar processes for judging
(Figure 1a, b). The fact that these regions were not ident- ourselves and others, and the extent to which these pro-
ified in the vast majority of standard contrasts suggests cesses are dedicated to the processing of social information
that MPFC involvement might have been missed in prior as opposed to more general meta-cognitive functions used
work examining activity averaged across subjects and time when categorizing and re-representing affective and other
points. The coactivation of these networks suggests that types of input in a symbolic format, is currently a matter of
emotion understanding might in some cases involve the debate [6,32].
use of reflective cognition drawing on the MPFC to inter- In sum, the research surveyed in this section suggests
pret activity in networks supporting experiential proces- that understanding the emotions of others through MSA is
sing of emotions. supported by a distributed functional network including
Interestingly, some of the same regions involved in cingulate and insula regions that are important for
reflecting upon others’ emotional states are involved in stimulus-driven processing of social cues and their under-
reflecting upon our own emotions [6,26], consistent with lying intentions, in addition to a network of regions cen-
theories suggesting that in some cases we treat ourselves tered on the MPFC used to reflect upon and reason about
as an ‘other’ when making self-judgments [31]. The reverse them.
might also be true: we use information about our own
states and traits when we reflect upon the states and traits Emotional learning
of others who seem to be like ourselves. Thus, judgments The role of MSA in emotion is not limited to understanding
about known or similar, as compared with less familiar or emotions in the present moment but additionally helps us
dissimilar, others draw on medial frontal regions similar to to learn about emotion-eliciting events and also to
those used for self-referential processing [6,27]. Exactly form lasting impressions of others’ emotionally relevant
Figure 1. (a, b) Sagittal views of areas with increased connectivity with seed regions commonly active during self and other pain in the (a) AI and (b) ACC [15]. Activations
during the direct experience of pain are marked in red, and during the observation of others’ pain are marked in blue. Importantly, when observing others’ pain, activation in
the MPFC (circled) co-varied with activation in seed regions in both the AI {6,40,24}* and ACC {12,48,12}*. (c,d) Functional activation during an observational fear learning
task [35]; (c) shows a coronal view of activation in the right AI {–28, 15, –4}y when observing the pain response of a learning model to a shock. The adjacent graph shows that
the magnitude of this activation predicts the strength of the conditioned response (indexed by the skin conductance response) at a later time to a cue associated with the
pain of the learning model (P < 0.05). (d) A sagittal view of activation in the (1) MPFC {1,46,24}y and (2) ACC {3,27,32}y during the observation of the pain response of a
learning model to a shock. As in (c), adjacent graphs display the positive relationship between the magnitude of activation during observation and the subsequent
conditioned response (P = 0.08 and P < 0.05 for 1 and 2, respectively).z*x, y, z coordinates for local maxima in Montreal Neurological Institute (MNI) space; yx, y, z
coordinates for local maxima in Talairach space; zafter one individual who was an outlier was removed.
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dispositions. For example, watching another’s fear [50] or knowing that they are in pain [24] – perhaps
expression to an unfamiliar dog could provide valuable because of an expectation that the partner’s behavior will
information about potential danger, that individual’s be brought back in line with expected norms. It should be
anxious disposition or both. These abilities to learn from noted, however, that growing evidence suggests that the
and about others crucially depend on understanding amygdala and striatum are not simply ‘fear’ and ‘reward’
others’ emotions using both stimulus-driven and reflective systems, and instead are sensitive to the arousal-related
MSAs. and motivational properties of valenced stimuli in general
[51,52].
Learning from others The affective value of a social target is determined, of
Neuroscience models of emotional learning are based course, both by their dispositions and by situational vari-
primarily on studies of fear conditioning showing that ables [53]. An identical punch might be taken as aggressive
the amygdala is crucial for learning through direct experi- or playful, for example, depending on one’s assessment of
ence which stimuli predict aversive outcomes [33,34]. the puncher’s intent. Contextual information that precedes
Emotional learning can also take place through indirect or follows initial stimulus-driven assessments might flex-
means, however, such as verbal communication and obser- ibly constrain and update them using bidirectional inter-
vation. Although these social–emotional routes to learning connections between the amygdala, striatum and
are crucial to everyday life for most humans [35], their orbitofrontal cortex (OFC) [54–56]. For example, OFC
neural bases have only recently begun to be explored damage might cause an individual to be unable to appreci-
[36,37]. ate faux pas, or to consider that the amount they tease
A common example is observational fear learning in someone, or are praised by them, is contextually inap-
which one vicariously learns to fear a stimulus that elicits propriate [54,56,57]. In such situations, OFC damage
expressions of fear in a conspecific. Cross-species research impairs the ability quickly and implicitly to use MSAs
demonstrates that learning fear through observing others (e.g. my girlfriend is embarrassed. . .) to regulate
shares behavioral [38,39] and neural features with con- moment-to-moment behavior (. . .so I should stop teasing
ditioned fear, including involvement of the amygdala her). By contrast, rostral and dorsal MPFC might support
[37,40]. Although this suggests that low-level stimulus- explicit MSAs used when reflecting upon the intentions
driven processes have an important role in observational behind and consequences of actions, as evidenced by its
fear learning across species, recent work in humans activation during strategic games [50,58] and when for-
suggests that, in addition to explicit knowledge about giving others’ transgressions [59].
the stimulus contingencies, fear learning through obser- Taken together, current work suggests that both rapid
vation might also involve higher-level reflective MSAs. and reflective MSAs support emotional learning from and
Olsson et al. [37] found that overlapping regions of the about others. As the complexity of required MSAs
amygdala, AI and ACC were active during both observa- increases, processing might move from stimulus-driven
tional learning and subsequent expression of fear subcortical to orbitofrontal regions and on to rostral and
responses, whereas the dorsal MPFC was active only dorsal MPFC regions if processing becomes explicitly eva-
during observation of another’s distress. Importantly, luative or reflective.
the magnitude of the conditioned response was predicted
by activity in the AI, ACC and dorsal MPFC (Figure 1c,d). Regulation of emotional responses
This suggests that shared representations supporting The MSA processes used for emotion understanding and
experiential understanding of emotion – in addition to learning also enable us adaptively to regulate our own
regions supporting reflective MSAs – jointly support emotional responses. To date, studies have investigated
social–emotional learning (Figure 1c,d). primarily the use of higher-level MSAs to regulate emotion
in two ways.
Learning about others The first ‘situation focused’ or ‘other focused’ strategy
The two types of MSAs that support learning from others involves reinterpreting the situational meaning of others’
also provide crucial diagnostic information about others’ intentions or feelings, as when, for example, thinking
stable social–emotional dispositions. Consider a social positively or negatively about the dispositions (she is
interaction that unfolds over time. During the initial hearty or weak) and future emotions (she will feel fine
moments of contact, stimulus-driven systems might assess or get worse) experienced by someone who is sick and in
the affective value of social targets with varying degrees of pain [60–62]. Interestingly, recent work suggests that
complexity. For example, the simple perception or evalu- simply making an attribution about the feelings of another
ation of either attractive or potentially threatening and person can have the unintended consequence of disrupting
untrustworthy faces activates either striatal regions impli- amygdala-mediated negative evaluations of them [63,64].
cated in reward and reinforcement learning [41] or the One reason for this might be that MSAs can direct atten-
amygdala and AI regions implicated in aversive learning, tion to the nonthreatening intentions (e.g. thinking about
as described earlier [42–45]. With repeated interaction, their food preferences) of a social target, thereby disambig-
imaging studies suggest that the striatum might encode uating them as potential sources of threat.
which actions produce desired social outcomes, consistent The second ‘self-focused’ strategy involves mentally
with its general role in reinforcement learning [41,46]. manipulating one’s personal connection to an emotionally
Striatum activity accompanies both cooperation and trust charged situation, as when, for example, one experiences
[46–49] – but also punishing a previously unfair partner aversive events from the simulated perspective of an
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Figure 2. A functional–anatomical organization of regions supporting the role of MSA in emotion. (a) Midline regions (e.g. MPFC) interconnected with emotion centers
support representations of internal states and might be coding emotional qualities of MSAs. By contrast, lateral regions [e.g. the lateral prefrontal cortex (LPFC) and TPJ]
interconnected with visuospatial centers support externally generated representations and might be coding cognitive aspects of MSA. (b) Closely aligned to the midline
section along with the insula (1), posterior regions [e.g. the posterior cingulate cortex (PCC), posterior insula (PI) and the mACC] support simple ‘first-order’ sensory aspects
of MSA, whereas representational complexity increases as the information is re-represented in more anterior regions (e.g. MPFC); (2) ventral regions [e.g. the amygdala (A),
OFC, striatum (Stri) and ventral MPFC (vMPFC)] are predominantly engaged in stimulus-driven processes, whereas dorsal regions [e.g. dorsal MPFC (dMPFC) and LPFC]
support performance monitoring and reflective processes of MSA. Abbreviation: cogn, cognitive; R, right.
objective and detached third person observer [65–67]. key role integrating information about the internal state
Although each strategy can modulate stimulus-driven of the body with higher-level mental state knowledge
amygdala activity, they seem to depend differentially upon needed to categorize affective states. Finally, as processing
complementary PFC regions: the MPFC – which receives moves from ventral to dorsal regions, it becomes less
direct inputs about the internal state of the body – might be stimulus driven and increasingly controlled and reflective,
relatively more important for self-focused regulation, enabling one to judge explicitly and be aware of one’s own
whereas other-focused regulation might depend more on or others’ emotional states. Given the early stages of
ventrolateral PFC regions used to select from memory research in this area, of course, the functional distinctions
information that helps to interpret others’ feelings [6]. drawn between medial-lateral, posterior-anterior and ven-
In sum, it seems that MSAs can regulate emotion either tral-dorsal regions are by necessity highly simplified and
through reinterpretations of others’ feelings or by simu- heuristic. It is expected that continued research will be
lating what it would be like to be experiencing the event crucial for their further specification.
from a third person perspective. These strategies might
differentially depend on medial and lateral regions of the Future directions
PFC, respectively. This survey of research on the neural bases of MSA in
emotion understanding, learning and regulation provides
A neural framework for the role of social cognition a framework for understanding current work but also
in emotion highlights how much there remains to be clarified in future
One way to understand the relationship between social research. At least four types of question will be important
cognition and emotion is to delineate the way in which the to address.
processes and mental representations underlying them are The first concerns the fact that research has focused on
distributed along general functional axes in the brain how the average person perceives emotions in static social
[30,68]. Based on the preceding review, we propose that stimuli, but less is known about how dispositional or
the role of social cognition – and MSA in particular – in situational motivations (e.g. to seek affiliation or fear
emotion can be understood in terms of three related but rejection, or be empathic versus competitive) might influ-
distinct dimensions of functional–anatomic organization. ence the neural systems supporting emotion understand-
The proposed framework should be viewed as complemen- ing, learning and regulation during real-time social
tary to previously formulated functional–anatomical interaction. Methods and approaches are now being devel-
models, which have attempted to capture a broader array oped to address these issues [48,69].
of social cognitive phenomena and have often done so along Second, an interactive approach will also be important
two dimensions [30,68]. According to the scheme proposed for the analysis of data, to clarify how different components
here (Figure 2, Box 3), lateral regions preferentially pro- of the functional networks supporting MSA work together
cess information about external inputs, whereas medial in social cognitive and emotional attributions. Indeed, the
regions have an essential role in MSA by representing fact that both simple and complex MSAs can be impaired
information about internal states [68]. Along with following damage to just one of the regions described ear-
the AI, posterior medial regions such as the mACC lier [54,70,71], and that each region might have general
represent body state information that is represented with functional roles beyond MSA [26,32], makes it clear that
increasing complexity as processing moves anteriorly understanding time- and context-varying interactions be-
towards the frontal pole and BA 10 [30]. BA 10 has a tween regions will be essential [15].
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