Neural signatures of social inferences predict the number of real-life social contacts and autism severity.

We regularly infer other people's thoughts and feelings from observing their actions, but how this ability contributes to successful social behavior and interactions remains unknown. We show that neural activation patterns during social inferences obtained in the laboratory predict the number of social contacts in the real world, as measured by the social network index, in three neurotypical samples (total n = 126) and one sample of autistic adults (n = 23). We also show that brain patterns during social inference generalize across individuals in these groups. Cross-validated associations between brain activations and social inference localize selectively to the right posterior superior temporal sulcus and were specific for social, but not nonsocial, inference. Activation within this same brain region also predicts autism-like trait scores from questionnaires and autism symptom severity. Thus, neural activations produced while thinking about other people's mental states predict variance in multiple indices of social functioning in the real world.

The neuroscience of understanding the emotions of others.

We cannot help but impute emotions to the behaviors of others, and constantly infer not only what others are feeling, but also why they feel that way. The comprehension of other people's emotional states is computationally complex and difficult, requiring the flexible, context-sensitive deployment of cognitive operations that encompass rapid orienting to, and recognition of, emotionally salient cues; classification of emotions into culturally-learned categories; and using an abstract theory of mind to reason about what caused the emotion, what future actions the person might be planning, and what we should do next in response. This review summarizes what neuroscience data - primarily functional neuroimaging data - has so far taught us about the cognitive architecture enabling emotion understanding in its various forms.

A new look at domain specificity: insights from social neuroscience.

The concept of domain specificity - which suggests that some aspects of neural processing are specialized for particular types of stimuli - has been invoked to explain a range of cognitive phenomena, including language, face perception and theory of mind, and has been a hallmark of theories of cognitive architecture. More recent usage of this concept draws on neuroscientific data and, in particular, on work in social neuroscience. A critical examination of the part that the concept of domain specificity has played in theories of human brain function leads us to suggest a new view according to which domain specificity pertains to centrally generated constraints on information processing that can be both dynamic and context sensitive.

The neural basis of understanding the expression of the emotions in man and animals.

Humans cannot help but attribute human emotions to non-human animals. Although such attributions are often regarded as gratuitous anthropomorphisms and held apart from the attributions humans make about each other's internal states, they may be the product of a general mechanism for flexibly interpreting adaptive behavior. To examine this, we used functional magnetic resonance imaging (fMRI) in humans to compare the neural mechanisms associated with attributing emotions to humans and non-human animal behavior. Although undergoing fMRI, participants first passively observed the facial displays of human, non-human primate and domestic dogs, and subsequently judged the acceptability of emotional (e.g. 'annoyed') and facial descriptions (e.g. 'baring teeth') for the same images. For all targets, emotion attributions selectively activated regions in prefrontal and anterior temporal cortices associated with causal explanation in prior studies. These regions were similarly activated by both human and non-human targets even during the passive observation task; moreover, the degree of neural similarity was dependent on participants' self-reported beliefs in the mental capacities of non-human animals. These results encourage a non-anthropocentric view of emotion understanding, one that treats the idea that animals have emotions as no more gratuitous than the idea that humans other than ourselves do.

The neural basis of conceptualizing the same action at different levels of abstraction.

People can conceptualize the same action (e.g. 'riding a bike') at different levels of abstraction (LOA), where higher LOAs specify the abstract motives that explain why the action is performed (e.g. 'getting exercise'), while lower LOAs specify the concrete steps that indicate how the action is performed (e.g. 'gripping handlebars'). Prior neuroimaging studies have shown that why and how questions about actions differentially activate two cortical networks associated with mental-state reasoning and action representation, respectively; however, it remains unknown whether this is due to the differential demands of the questions per se or to the shifts in LOA those questions produce. We conducted functional magnetic resonance imaging while participants judged pairs of action phrases that varied in LOA and that could be framed either as a why question (Why ride a bike? Get exercise.) or a how question (How to get exercise? Ride a bike.). Question framing (why vs how) had no effect on activity in regions of the two networks. Instead, these regions uniquely tracked parametric variation in LOA, both across and within trials. This suggests that the human capacity to understand actions at different LOA is based in the relative activity of two cortical networks.

Folk explanations of behavior: a specialized use of a domain-general mechanism.

People typically explain others' behaviors by attributing them to the beliefs and motives of an unobservable mind. Although such attributional inferences are critical for understanding the social world, it is unclear whether they rely on processes distinct from those used to understand the nonsocial world. In the present study, we used functional MRI to identify brain regions associated with making attributions about social and nonsocial situations. Attributions in both domains activated a common set of brain regions, and individual differences in the domain-specific recruitment of one of these regions--the dorsomedial prefrontal cortex (DMPFC)--correlated with attributional accuracy in each domain. Overall, however, the DMPFC showed greater activation for attributions about social than about nonsocial situations, and this selective response to the social domain was greatest in participants who reported the highest levels of social expertise. We conclude that folk explanations of behavior are an expert use of a domain-general cognitive ability.

Amygdala lesions do not compromise the cortical network for false-belief reasoning.

The amygdala plays an integral role in human social cognition and behavior, with clear links to emotion recognition, trust judgments, anthropomorphization, and psychiatric disorders ranging from social phobia to autism. A central feature of human social cognition is a theory-of-mind (ToM) that enables the representation other people's mental states as distinct from one's own. Numerous neuroimaging studies of the best studied use of ToM--false-belief reasoning--suggest that it relies on a specific cortical network; moreover, the amygdala is structurally and functionally connected with many components of this cortical network. It remains unknown whether the cortical implementation of any form of ToM depends on amygdala function. Here we investigated this question directly by conducting functional MRI on two patients with rare bilateral amygdala lesions while they performed a neuroimaging protocol standardized for measuring cortical activity associated with false-belief reasoning. We compared patient responses with those of two healthy comparison groups that included 480 adults. Based on both univariate and multivariate comparisons, neither patient showed any evidence of atypical cortical activity or any evidence of atypical behavioral performance; moreover, this pattern of typical cortical and behavioral response was replicated for both patients in a follow-up session. These findings argue that the amygdala is not necessary for the cortical implementation of ToM in adulthood and suggest a reevaluation of the role of the amygdala and its cortical interactions in human social cognition.

The default mode of human brain function primes the intentional stance.

Humans readily adopt an intentional stance to other people, comprehending their behavior as guided by unobservable mental states such as belief, desire, and intention. We used fMRI in healthy adults to test the hypothesis that this stance is primed by the default mode of human brain function present when the mind is at rest. We report three findings that support this hypothesis. First, brain regions activated by actively adopting an intentional rather than nonintentional stance to a social stimulus were anatomically similar to those demonstrating default responses to fixation baseline in the same task. Second, moment-to-moment variation in default activity during fixation in the dorsomedial PFC was related to the ease with which participants applied an intentional--but not nonintentional--stance to a social stimulus presented moments later. Finally, individuals who showed stronger dorsomedial PFC activity at baseline in a separate task were generally more efficient when adopting the intentional stance and reported having greater social skills. These results identify a biological basis for the human tendency to adopt the intentional stance. More broadly, they suggest that the brain's default mode of function may have evolved, in part, as a response to life in a social world.

Deconstructing and reconstructing theory of mind.

Usage of the term 'theory of mind' (ToM) has exploded across fields ranging from developmental psychology to social neuroscience and psychiatry research. However, its meaning is often vague and inconsistent, its biological bases are a subject of debate, and the methods used to study it are highly heterogeneous. Most crucially, its original definition does not permit easy downward translation to more basic processes such as those studied by behavioral neuroscience, leaving the interpretation of neuroimaging results opaque. We argue for a reformulation of ToM through a systematic two-stage approach, beginning with a deconstruction of the construct into a comprehensive set of basic component processes, followed by a complementary reconstruction from which a scientifically tractable concept of ToM can be recovered.

Validating the Why/How contrast for functional MRI studies of Theory of Mind.

The ability to impute mental states to others, or Theory of Mind (ToM), has been the subject of hundreds of neuroimaging studies. Although reviews and meta-analyses of these studies have concluded that ToM recruits a coherent brain network, mounting evidence suggests that this network is an abstraction based on pooling data from numerous studies, most of which use different behavioral tasks to investigate ToM. Problematically, this means that no single behavioral task can be used to reliably measure ToM Network function as currently conceived. To make ToM Network function scientifically tractable, we need standardized tasks capable of reliably measuring specific aspects of its functioning. Here, our goal is to validate the Why/How Task for this purpose. Several prior studies have found that when compared to answering how-questions about another person's behavior, answering why-questions about that same behavior activates a network that is anatomically consistent with meta-analytic definitions of the ToM Network. In the version of the Why/How Task presented here, participants answer yes/no Why (e.g., Is the person helping someone?) and How (e.g., Is the person lifting something?) questions about pretested photographs of naturalistic human behaviors. Across three fMRI studies, we show that the task elicits reliable performance measurements and modulates a left-lateralized network that is consistently localized across studies. While this network is convergent with meta-analyses of ToM studies, it is largely distinct from the network identified by the widely used False-Belief Localizer, the most common ToM task. Our new task is publicly available, and can be used as an efficient functional localizer to provide reliable identification of single-subject responses in most regions of the network. Our results validate the Why/How Task, both as a standardized protocol capable of producing maximally comparable data across studies, and as a flexible foundation for programmatic research on the neurobiological foundations of a basic manifestation of human ToM.

Reverse-correlating mental representations of sex-typed bodies: the effect of number of trials on image quality.

Sex categorization is a critical process in social perception. While psychologists have long theorized that perceivers have distinct mental representations of men and women that help them to achieve efficient sex categorizations, researchers have only recently begun using reverse-correlation to visualize the content of these mental representations. The present research addresses two issues concerning this relatively new methodological tool. First, previous studies of reverse-correlation have focused almost exclusively on perceivers' mental representations of faces. Our study demonstrates that this technique can also be used to visualize mental representations of sex-typed bodies. Second, most studies of reverse-correlation have employed a relatively large number of trials (1000+) to capture perceivers' mental representations of a given category. Our study demonstrated that, at least for sex-typed representations of bodies, high quality reverse-correlation images can be obtained with as few as 100 trials. Overall, our findings enhance knowledge of reverse-correlation methodology in general and sex categorization in particular, providing new information for researchers interested in using this technique to understand the complex processes underlying social perception.

The busy social brain: evidence for automaticity and control in the neural systems supporting social cognition and action understanding.

Much social-cognitive processing is believed to occur automatically; however, the relative automaticity of the brain systems underlying social cognition remains largely undetermined. We used functional MRI to test for automaticity in the functioning of two brain systems that research has indicated are important for understanding other people's behavior: the mirror neuron system and the mentalizing system. Participants remembered either easy phone numbers (low cognitive load) or difficult phone numbers (high cognitive load) while observing actions after adopting one of four comprehension goals. For all four goals, mirror neuron system activation showed relatively little evidence of modulation by load; in contrast, the association of mentalizing system activation with the goal of inferring the actor's mental state was extinguished by increased cognitive load. These results support a dual-process model of the brain systems underlying action understanding and social cognition; the mirror neuron system supports automatic behavior identification, and the mentalizing system supports controlled social causal attribution.

The phenomenology of error processing: the dorsal ACC response to stop-signal errors tracks reports of negative affect.

A reliable observation in neuroimaging studies of cognitive control is the response of dorsal ACC (dACC) to events that demand increased cognitive control (e.g., response conflicts and performance errors). This observation is apparently at odds with a comparably reliable association of the dACC with the subjective experience of negative affective states such as pain, fear, and anxiety. Whereas "affective" associates of the dACC are based on studies that explicitly manipulate and/or measure the subjective experience of negative affect, the "cognitive" associates of dACC are based on studies using tasks designed to manipulate the demand for cognitive control, such as the Stroop, flanker, and stop-signal tasks. Critically, extant neuroimaging research has not systematically considered the extent to which these cognitive tasks induce negative affective experiences and, if so, to what extent negative affect can account for any variance in the dACC response during task performance. While undergoing fMRI, participants in this study performed a stop-signal task while regularly reporting their experience of performance on several dimensions. We observed that within-subject variability in the dACC response to stop-signal errors tracked changes in subjective frustration throughout task performance. This association remained when controlling for within-subject variability in subjective reports of cognitive engagement and several performance-related variables indexing task difficulty. These results fit with existing models characterizing the dACC as a hub for monitoring ongoing behavior and motivating adjustments when necessary and further emphasize that such a function may be linked to the subjective experience of negative affect.

Dissociating modality-specific and supramodal neural systems for action understanding.

The neural basis of action understanding in humans remains disputed, with some research implicating the putative mirror neuron system (MNS) and some a mentalizing system (MZS) for inferring mental states. The basis for this dispute may be that action understanding is a heterogeneous construct: actions can be understood from sensory information about body movements or from language about action, and with the goal of understanding the implementation ("how") or motive ("why") of an action. Although extant research implicates the MNS in understanding implementation and the MZS in understanding motive, it remains unknown to what extent these systems subserve modality-specific or supramodal functions in action understanding. While undergoing fMRI, 21 volunteers considered the implementation ("How is she doing it?") and motive ("Why is she doing it?") for actions presented in video or text. Bilateral parietal and right frontal areas of the MNS showed a modality-specific association with perceiving actions in videos, while left-hemisphere MNS showed a supramodal association with understanding implementation. Largely left-hemisphere MZS showed a supramodal association with understanding motive; however, connectivity among the MZS and MNS during the inference of motive was modality specific, being significantly stronger when motive was understood from actions in videos compared to text. These results support a tripartite model of MNS and MZS contributions to action understanding, where distinct areas of the MNS contribute to action perception ("perceiving what") and the representation of action implementation ("knowing how"), while the MZS supports an abstract, modality-independent representation of the mental states that explain action performance ("knowing why").

Evidence for social working memory from a parametric functional MRI study.

Keeping track of various amounts of social cognitive information, including people's mental states, traits, and relationships, is fundamental to navigating social interactions. However, to date, no research has examined which brain regions support variable amounts of social information processing ("social load"). We developed a social working memory paradigm to examine the brain networks sensitive to social load. Two networks showed linear increases in activation as a function of increasing social load: the medial frontoparietal regions implicated in social cognition and the lateral frontoparietal system implicated in nonsocial forms of working memory. Of these networks, only load-dependent medial frontoparietal activity was associated with individual differences in social cognitive ability (trait perspective-taking). Although past studies of nonsocial load have uniformly found medial frontoparietal activity decreases with increasing task demands, the current study demonstrates these regions do support increasing mental effort when such effort engages social cognition. Implications for the etiology of clinical disorders that implicate social functioning and potential interventions are discussed.

Ascribing beliefs to ingroup and outgroup political candidates: neural correlates of perspective-taking, issue importance and days until the election.

We used the five weeks leading up to the 2008 presidential election as a backdrop to examine the ways that the brain processes attitudes and beliefs under different circumstances. We examined individual differences in personal issue importance and trait perspective-taking, as well as the temporal context in which attitude representation took place (i.e. number of days until the election). Finally, we examined the extent to which similar or dissimilar processes were recruited when considering the attitudes of political ingroup and outgroup candidates. Brain regions involved in social cognition and theory of mind, and to a lesser extent the limbic system, were modulated by these factors. Higher issue importance led to greater recruitment of neural regions involved in social cognition, across target perspectives. Higher trait perspective-taking was also associated with greater recruitment of several regions involved in social cognition, but differed depending on target perspective; greater activity was observed in prefrontal regions associated with social cognition when considering the perspective of one's own candidate compared with the opponent, and this effect was amplified closer to the election. Taken together, these results highlight ways in which ability and motivational relevance modulate socio-affective processing of the attitudes of others.

An integrative model of the neural systems supporting the comprehension of observed emotional behavior.

Understanding others' emotions requires both the identification of overt behaviors ("smiling") and the attribution of behaviors to a cause ("friendly disposition"). Previous research suggests that whereas emotion identification depends on a cortical mirror system that enables the embodiment of observed motor behavior within one's own motor system, causal attribution for emotion depends on a separate cortical mentalizing system, so-named because its function is associated with mental state representation. We used fMRI to test an Identification-Attribution model of mirror and mentalizing system contributions to the comprehension of emotional behavior. Normal volunteers watched a set of ecologically valid videos of human emotional displays. During each viewing, volunteers either identified an emotion-relevant motor behavior (explicit identification) or inferred a plausible social cause (explicit attribution). These explicit identification and attribution goals strongly distinguished activity in the mirror and mentalizing systems, respectively. However, frontal mirror areas, though preferentially engaged by the identification goal, nevertheless exhibited activation when observers possessed the attribution goal. One of these areas-right posterior inferior frontal gyrus-demonstrated effective connectivity with areas of the mentalizing system during attributional processing. These results support an integrative model of the neural systems supporting the comprehension of emotional behavior, where the mirror system helps facilitate the rapid identification of emotional expressions that then serve as inputs to attributional processing in the mentalizing system.

Identifying the what, why, and how of an observed action: an fMRI study of mentalizing and mechanizing during action observation.

Humans commonly understand the unobservable mental states of others by observing their actions. Embodied simulation theories suggest that this ability may be based in areas of the fronto-parietal mirror neuron system, yet neuroimaging studies that explicitly investigate the human ability to draw mental state inferences point to the involvement of a “mentalizing" system consisting of regions that do not overlap with the mirror neuron system. For the present study, we developed a novel action identification paradigm that allowed us to explicitly investigate the neural bases of mentalizing observed actions. Across repeated viewings of a set of ecologically valid video clips of ordinary human actions, we manipulated the extent to which participants identified the unobservable mental states of the actor (mentalizing) or the observable mechanics of their behavior (mechanizing). Although areas of the mirror neuron system did show an enhanced response during action identification, its activity was not significantly modulated by the extent to which the observers identified mental states. Instead, several regions of the mentalizing system, including dorsal and ventral aspects of medial pFC, posterior cingulate cortex, and temporal poles, were associated with mentalizing actions, whereas a single region in left lateral occipito-temporal cortex was associated with mechanizing actions. These data suggest that embodied simulation is insufficient to account for the sophisticated mentalizing that human beings are capable of while observing another and that a different system along the cortical midline and in anterior temporal cortex is involved in mentalizing an observed action.

Dissociable neural systems support retrieval of how and why action knowledge.

In everyday discourse, people typically represent actions in one of two ways: how they are performed or why they are performed. In the present study, we determined the neural systems that support these natural modes of representing actions. Participants underwent functional magnetic resonance imaging while identifying how and why people perform various familiar actions. Identifying how actions are performed produced activity in premotor areas that support the execution of actions and in higher-order visual areas that support the perception of action-related objects; this finding supports an embodied view of action knowledge. However, identifying why actions are performed preferentially engaged areas of the brain associated with representing and reasoning about mental states; these areas were right temporoparietal junction, precuneus, dorsomedial prefrontal cortex, and posterior superior temporal sulcus. Our results suggest that why action knowledge is not sufficiently constituted by information in motor and visual systems, but requires a system for representing states of mind, which do not have reliable motor correlates or visual appearance.