Social Neuroscience

This study used fMRI to investigate the functioning of the Theory of Mind (ToM) cortical network in autism during the viewing of animations that in some conditions entailed the attribution of a mental state to animated geometric figures. At the cortical level, mentalizing (attribution of metal states) is underpinned by the coordination and integration of the components of the ToM network, which include the medial frontal gyrus, the anterior paracingulate, and the right temporoparietal junction. The pivotal new finding was a functional underconnectivity (a lower degree of synchronization) in autism, especially in the connections between frontal and posterior areas during the attribution of mental states. In addition, the frontal ToM regions activated less in participants with autism relative to control participants. In the autism group, an independent psychometric assessment of ToM ability and the activation in the right temporoparietal junction were reliably correlated. The results together provide new evidence for the biological basis of atypical processing of ToM in autism, implicating the underconnectivity between frontal regions and more posterior areas.

Moral judgment depends critically on theory of mind (ToM), reasoning about mental states such as beliefs and intentions. People assign blame for failed attempts to harm and offer forgiveness in the case of accidents. Here we use fMRI to investigate the role of ToM in moral judgment of harmful vs. helpful actions. Is ToM deployed differently for judgments of blame vs. praise? Participants evaluated agents who produced a harmful, helpful, or neutral outcome, based on a harmful, helpful, or neutral intention; participants made blame and praise judgments. In the right temporo-parietal junction (right TPJ), and, to a lesser extent, the left TPJ and medial prefrontal cortex, the neural response reflected an interaction between belief and outcome factors, for both blame and praise judgments: The response in these regions was highest when participants delivered a negative moral judgment, i.e., assigned blame or withheld praise, based solely on the agent's intent (attempted harm, accidental help). These results show enhanced attention to mental states for negative moral verdicts based exclusively on mental state information.

Social behavior and desire for social relationships have been independently linked to the serotonergic system, the prefrontal cortex, especially the orbitofrontal cortex (OFC), and the anterior cingulate cortex (ACC). The goal of this study was to explore the role of serotonin 5HT(2A) receptors in these brain regions in forming and maintaining close interpersonal relationships. Twenty-four healthy subjects completed the Temperament and Character Inventory (TCI) prior to undergoing [(18)F]setoperone brain positron emission tomography (PET) to measure serotonin 5HT(2A) receptor availability within the OFC (BA 11 and 47) and ACC (BA 32). We explored the relationship between desire for social relationships, as measured by the TCI reward dependence (RD) scale, and 5HT(2A) receptor non-displaceable binding potential (BP(nd)) in these regions. Scores of RD were negatively correlated with 5HT(2A) BP(nd) in the ACC (BA 32, r = -.528, p = .012) and OFC (BA 11, r = -.489, p = .021; BA 47, r = -.501, p = .017). These correlations were corroborated by a voxel-wise analysis. These results suggest that the serotonergic system may have a regulatory effect on the OFC and ACC for establishing and maintaining social relationships.

The retention of first-order theory of mind (ToM) despite severe loss of grammar has been reported in two patients with left hemisphere brain damage (Varley & Siegal, 200033. Varley , R. and Siegal , M. 2000. Evidence for cognition without grammar from causal reasoning and “theory of mind” in an agrammatic aphasic patient. Current Biology, 10: 723–726. [PubMed], [Web of Science ®], [CSA]View all references; Varley, Siegal, & Want, 200134. Varley , R. , Siegal , M. and Want , S. C. 2001. Severe impairment in grammar does not preclude theory of mind. Neurocase, 7: 489–493. [Taylor & Francis Online], [PubMed], [Web of Science ®], [CSA]View all references). We report a third, and more detailed, case study. Patient PH shows significant general language impairment, and severe grammatical impairment similar to that reported in previous studies. In addition we were able to show that PH's impairment extends to grammatical constructions most closely related to ToM in studies of children (embedded complement clauses and relative clauses). Despite this, PH performed almost perfectly on first-order false belief tasks and on a novel nonverbal second-order false belief task. PH was also successful on a novel test of “ToM semantics” that required evaluation of the certainty implied by different mental state terms. The data strongly suggest that grammar is not a necessary source of structure for explicit ToM reasoning in adults, but do not rule out a critical role for “ToM semantics.” In turn this suggests that the relationship observed between grammar and ToM in studies of children is the result of an exclusively developmental process.

A large body of evidence links altered opioid signaling with changes in social behavior in animals. However, few studies have attempted to determine whether similar links exist in humans. Here we investigate whether a common polymorphism (A118G) in the mu-opioid receptor gene (OPRM1) is associated with alterations in personality traits linked to affiliative behavior and attachment. In a mixed sample (N = 214) of adult healthy volunteers and psychiatric patients, we analyzed the association between the A118G polymorphism of the OPRM1 and two different psychological constructs reflecting individual differences in the capacity to experience social reward. Compared to individuals expressing only the major allele (A) of the A118G polymorphism, subjects expressing the minor allele (G) had an increased tendency to become engaged in affectionate relationships, as indicated by lower scores on a self-report measure of avoidant attachment, and experienced more pleasure in social situations, as indicated by lower scores on a self-report measure of social anhedonia. The OPRM1 variation accounted for about 3.5% of the variance in the two measures. The significant association between the A118G polymorphism and social hedonic capacity was independent of the participants' mental health status. The results reported here are in agreement with the brain opioid hypothesis of social attachment and the established role of opioid transmission in mediating affiliative behavior.

Patients with schizophrenia often show abnormal social interactions, which may explain their social exclusion behaviors. This study aimed to elucidate patients' brain responses to social rejection in an interactive situation. Fifteen patients with schizophrenia and 16 healthy controls participated in the functional magnetic resonance imaging experiment with the virtual handshake task, in which socially interacting contents such as acceptance and refusal of handshaking were implemented. Responses to the refusal versus acceptance conditions were evaluated and compared between the two groups. Controls revealed higher activity in the refusal condition compared to the acceptance condition in the right superior temporal sulcus, whereas patients showed higher activity in the prefrontal regions, including the frontopolar cortex. In patients, contrast activities of the right superior temporal sulcus were inversely correlated with the severity of schizophrenic symptoms, whereas contrast activities of the left frontopolar cortex were positively correlated with the current anxiety scores. The superior temporal sulcus hypoactivity and frontopolar hyperactivity of patients with schizophrenia in social rejection situations may suggest the presence of mentalizing deficits in negative social situations and inefficient processes of socially aberrant stimuli, respectively. These abnormalities may be one of the neural bases of distorted or paranoid beliefs in schizophrenia.

Empathy is defined as an individually varying but stable personality trait. To our knowledge this notion seems questionable considering recent studies proving neuronal plasticity not only in childhood and adolescence but over the whole lifespan. We propose a model in which an individual's basic empathic abilities-arising from genetic factors, brain maturation, and early attachment experiences -are continually modulated by the intensity, continuity, and frequency of interpersonal socio-emotional stimulation and challenges. We assume neural processes and their underlying neural structures being modified by social and socio-emotional stimulation. Continuous social interactions should produce noticeable effects on the empathic abilities of an individual independent of age or brain maturation level. In particular, empathic abilities should be learnable and expandable beyond specific developmental windows. To elucidate this hypothesis we surveyed empathy measures of students of various professions with the help of a new instrument, the Questionnaire of Cognitive and Affective Empathy (QCAE) categorizing them into three different groups depending on their subsequent occupational fields: medical students, students of academic social professions, and a control group. Results indicate that continuous socio-emotional stimulation could increase empathic abilities potentially leading to learning effects.

To identify the brain regions involved in the interpretation of intentional movement by patients with schizophrenia, we investigated the association between cerebral gray matter (GM) volumes and performance on a theory of mind (ToM) task using voxel-based morphometry. Eighteen patients with schizophrenia and thirty healthy controls participated in the study. Participants were given a moving shapes task that employs the interpretation of intentional movement. Verbal descriptions were rated according to intentionality. ToM performance deficits in patients were found to be positively correlated with GM volume reductions in the superior temporal sulcus and medial prefrontal cortex. Our findings confirm that divergent brain regions contribute to mentalizing abilities and that GM volume reductions impact behavioral deficits in patients with schizophrenia.

The two studies reported in this article are an extension of the neuroimaging study by Ganis et al. (2003), which provided evidence that different types of lies arise from different cognitive processes. We examined the initial response times (IRTs) to questions answered both deceptively and truthfully. We considered four types of deceptive responses: a coherent set of rehearsed, memorized lies about a life experience; a coherent set of lies spontaneously created about a life experience; a set of isolated lies involving self-knowledge; and a set of isolated lies involving knowledge of another person. We assessed the difference between truthful and deceptive IRTs. Scores from cognitive tasks included in the MiniCog Rapid Assessment Battery (MRAB) were significant predictors of IRT differences. Each type of lie was predicted by a distinct set of MRAB scores. These results provide further evidence that deception is a multifaceted process and that different kinds of lies arise from the operation of different cognitive processes.

Schizophrenia is associated with abnormal cortical activation during theory of mind (ToM), as demonstrated by several fMRI or PET studies. Electrical and temporal characteristics of these abnormalities, especially in the early stages, remain unexplored. Nineteen medicated schizophrenic patients and 21 healthy controls underwent magnetoencephalography (MEG) recording to measure brain response evoked by nonverbal stimuli requiring mentalizing. Three conditions based on comic-strips were contrasted: attribution of intentions to others (AI), physical causality with human characters (PCCH), and physical causality with objects (PCOB). Minimum norm localization was performed in order to select regions of interest (ROIs) within bilateral temporal and parietal regions that showed significant ToM-related activations in the control group. Time-courses of each ROI were compared across group and condition. Reduced cortical activation within the 200 to 600 ms time-window was observed in the selected regions in patients. Significant group by condition interactions (i.e., reduced modulation in patients) were found in right posterior superior temporal sulcus, right temporoparietal junction, and right inferior parietal lobule during attribution of intentions. As in healthy controls, the presence of characters elicited activation in patients' left posterior temporal regions and temporoparietal junction. No group difference on evoked responses' latencies in AI was found. In conclusion, ToM processes in the early stages are functionally impaired in schizophrenia. MEG provides a promising means to refine our knowledge on schizophrenic social cognitive disorders.

Infant faces elicit early, specific activity in the orbitofrontal cortex (OFC), a key cortical region for reward and affective processing. A test of the causal relationship between infant facial configuration and OFC activity is provided by naturally occurring disruptions to the face structure. One such disruption is cleft lip, a small change to one facial feature, shown to disrupt parenting. Using magnetoencephalography, we investigated neural responses to infant faces with cleft lip compared with typical infant and adult faces. We found activity in the right OFC at 140 ms in response to typical infant faces but diminished activity to infant faces with cleft lip or adult faces. Activity in the right fusiform face area was of similar magnitude for typical adult and infant faces but was significantly lower for infant faces with cleft lip. This is the first evidence that a minor change to the infant face can disrupt neural activity potentially implicated in caregiving.

Religious beliefs are both catchy and durable: they exhibit a high degree of adherence to our cognitive system, given their success of transmission and spreading throughout history. A prominent explanation for religion's cultural success comes from the "MCI hypothesis," according to which religious beliefs are both easy to recall and desirable to transmit because they are minimally counterintuitive (MCI). This hypothesis has been empirically tested at concept and narrative levels by recall measures. However, the neural correlates of MCI concepts remain poorly understood. We used the N400 component of the event-related brain potential as a measure of counterintuitiveness of violations comparing religious and non-religious sentences, both counterintuitive, when presented in isolation. Around 80% in either condition were core-knowledge violations. We found smaller N400 amplitudes for religious as compared to non-religious counterintuitive ideas, suggesting that religious ideas are less semantically anomalous. Moreover, behavioral measures revealed that religious ideas are not readily detected as unacceptable. Finally, systematic analyses of our materials, according to conceptual features proposed in cognitive models of religion, did not reveal any outstanding variable significantly contributing to these differences. Refinements of cognitive models of religion should elucidate which combination of factors renders an anomaly less counterintuitive and thus more suitable for recall and transmission.

In primates the gaze conveys important information about what others attend to and about their intentions. The ability to follow the gaze direction of conspecifics has been established for several primate species. It has been proposed to be a precursor for more complex cognitive skills related to mind reading. Studies in humans and other primates have shown that this behavior develops during the period between infancy and adulthood; however, the mechanisms responsible for its emergence are still unknown. In a series of experiments we investigated such mechanisms in macaques (Macaca nemestrina). Results show that juvenile macaques improve their ability to follow the gaze of a human experimenter and that adults' ability to follow gaze is more accurate than that of juveniles. Our data also show that this behavior can emerge as the result of learning processes. The discrepancy between the relatively long period of time needed for the full establishment of the gaze-following behavior and its high sensitivity to conditioning procedures may suggest that social experience and integration of this behavior with other social-cognitive skills are required for its development.

Self-construal priming modulates human behavior and associated neural activity. However, the neural activity associated with the self-construal priming procedure itself remains unknown. It is also unclear whether and how self-construal priming affects neural activity prior to engaging in a particular task. To address this gap, we scanned Chinese adults, using functional magnetic resonance imaging, during self-construal priming and a following resting state. We found that, relative to a calculation task, both interdependent and independent self-construal priming activated the ventral medial prefrontal cortex (MPFC) and the posterior cingulate cortex (PCC). The contrast of interdependent vs. independent self-construal priming also revealed increased activity in the dorsal MPFC and left middle frontal cortex. The regional homogeneity analysis of the resting-state activity revealed increased local synchronization of spontaneous activity in the dorsal MPFC but decreased local synchronization of spontaneous activity in the PCC when contrasting interdependent vs. independent self-construal priming. The functional connectivity analysis of the resting-state activity, however, did not show significant difference in synchronization of activities in remote brain regions between different priming conditions. Our findings suggest that accessible collectivistic/individualistic mind-set induced by self-construal priming is associated with modulations of both task-related and resting-state activity in the default mode network.

Oxytocin modulates many aspects of social cognition and behaviors, including maternal nurturing, social recognition and bonding. Natural variation in oxytocin receptor (OXTR) density in the nucleus accumbens (NAcc) is associated with variation in alloparental behavior, and artificially enhancing OXTR expression in the NAcc enhances alloparental behavior and pair bonding in socially monogamous prairie voles. Furthermore, infusion of an OXTR antagonist into the nucleus accumbens (NAcc) inhibits alloparental behavior and partner preference formation. However, antagonists can promiscuously interact with other neuropeptide receptors. To directly examine the role of OXTR signaling in social bonding, we used RNA interference to selectively knockdown, but not eliminate, OXTR in the NAcc of female prairie voles and examined the impact on social behaviors. Using an adeno-associated viral vector expressing a short hairpin RNA (shRNA) targeting Oxtr mRNA, we reduced accumbal OXTR density in female prairie voles from juvenile age through adulthood. Females receiving the shRNA vector displayed a significant reduction in alloparental behavior and disrupted partner preference formation. These are the first direct demonstrations that OXTR plays a critical role in alloparental behavior and adult social attachment, and suggest that natural variation in OXTR expression in this region alone can create variation in social behavior.

Observation of changes in autonomic arousal was one of the first methodologies used to detect deception. Electrodermal activity (EDA) is a peripheral measure of autonomic arousal and one of the primary channels used in polygraph exams. In an attempt to develop a more central measure to identify lies, the use of functional magnetic resonance imaging (fMRI) to detect deception is being investigated. We wondered if adding EDA to our fMRI analysis would improve our diagnostic ability. For our approach, however, adding EDA did not improve the accuracy in a laboratory-based deception task. In testing for brain regions that replicated as correlates of EDA, we did find significant associations in right orbitofrontal and bilateral anterior cingulate regions. Further work is required to test whether EDA improves accuracy in other testing formats or with higher levels of jeopardy.

A recently published study by the present authors reported evidence that functional changes in the anterior cingulate cortex within a sample of 96 criminal offenders who were engaged in a Go/No-Go impulse control task significantly predicted their rearrest following release from prison. In an extended analysis, we use discrimination and calibration techniques to test the accuracy of these predictions relative to more traditional models and their ability to generalize to new observations in both full and reduced models. Modest to strong discrimination and calibration accuracy were found, providing additional support for the utility of neurobiological measures in predicting rearrest.

Previous behavioral work suggests that processing information in relation to the self enhances subsequent item recognition. Neuroimaging evidence further suggests that regions along the cortical midline, particularly those of the medial prefrontal cortex (PFC), underlie this benefit. There has been little work to date, however, on the effects of self-referential encoding on source memory accuracy or whether the medial PFC might contribute to source memory for self-referenced materials. In the current study, we used fMRI to measure neural activity while participants studied and subsequently retrieved pictures of common objects superimposed on one of two background scenes (sources) under either self-reference or self-external encoding instructions. Both item recognition and source recognition were better for objects encoded self-referentially than self-externally. Neural activity predictive of source accuracy was observed in the medial PFC (Brodmann area 10) at the time of study for self-referentially but not self-externally encoded objects. The results of this experiment suggest that processing information in relation to the self leads to a mnemonic benefit for source level features, and that activity in the medial PFC contributes to this source memory benefit. This evidence expands the purported role that the medial PFC plays in self-referencing.

The motive to achieve success (MAS) and motive to avoid failure (MAF) are two different but classical kinds of achievement motivation. Though many functional magnetic resonance imaging studies have explored functional activation in motivation-related conditions, research has been silent as to the brain structures associated with individual differences in achievement motivation, especially with respect to MAS and MAF. In this study, the voxel-based morphometry method was used to uncover focal differences in brain structures related to MAS and MAF measured by the Mehrabian Achieving Tendency Scale in 353 healthy young Chinese adults. The results showed that the brain structures associated with individual differences in MAS and MAF were distinct. MAS was negatively correlated with regional gray matter volume (rGMV) in the medial prefrontal cortex (mPFC)/orbitofrontal cortex while MAF was negatively correlated with rGMV in the mPFC/subgenual cingulate gyrus. After controlling for mutual influences of MAS and MAF scores, MAS scores were found to be related to rGMV in the mPFC/orbitofrontal cortex and another cluster containing the parahippocampal gyrus and precuneus. These results may predict that compared with MAF, the generation process of MAS may be more complex and rational, thus in the real world, perhaps MAS is more beneficial to personal growth and guaranteeing the quality of task performance.

Recent neuroimaging studies on "theory of mind" have demonstrated that the medial prefrontal cortex (PFC) is involved when subjects are engaged in various kinds of mentalising tasks. Although a large number of neuroimaging studies have been published, a relatively small amount of neuropsychological evidence supports involvement of the medial PFC in theory of mind reasoning. We recruited two neurological cases with damage to the medial PFC and initially performed the standard neuropsychological assessments for intelligence, memory, and executive functions. To examine theory of mind performance in these two cases, four kinds of standard and advanced tests for theory of mind were used, including first- and second-order false belief tests, the strange stories test, and the faux pas recognition test. Both patients were also requested to complete the questionnaire for the autism-spectrum quotient. Neither case showed impairment on standard theory of mind tests and only mild impairments were seen on advanced theory of mind tests. This pattern of results is basically consistent with previous studies. The most interesting finding was that both cases showed personality changes after surgical operations, leading to characteristics of autism showing a lack of social interaction in everyday life. We discuss herein the possible roles of the medial PFC and emphasize the importance of using multiple approaches to understand the mechanisms of theory of mind and medial prefrontal functions.

Using event-related potentials, we investigated how the brain extracts information from another's face and translates it into relevant action in real time. In Study 1, participants made between-hand sex categorizations of sex-typical and sex-atypical faces. Sex-atypical faces evoked negativity between 250 and 550 ms (N300/N400 effects), reflecting the integration of accumulating sex-category knowledge into a coherent sex-category interpretation. Additionally, the lateralized readiness potential revealed that the motor cortex began preparing for a correct hand response while social category knowledge was still gradually evolving in parallel. In Study 2, participants made between-hand eye-color categorizations as part of go/no-go trials that were contingent on a target's sex. On no-go trials, although the hand did not actually move, information about eye color partially prepared the motor cortex to move the hand before perception of sex had finalized. Together, these findings demonstrate the dynamic continuity between person perception and action, such that ongoing results from face processing are immediately and continuously cascaded into the motor system over time. The preparation of action begins based on tentative perceptions of another's face before perceivers have finished interpreting what they just saw.

Performing an action and observing it activate the same internal representations of action. The representations are therefore shared between self and other (shared representations of action, SRA). But what exactly is shared? At what level within the hierarchical structure of the motor system do SRA occur? Understanding the content of SRA is important in order to decide what theoretical work SRA can perform. In this paper, we provide some conceptual clarification by raising three main questions: (i) are SRA semantic or pragmatic representations of action?; (ii) are SRA sensory or motor representations?; (iii) are SRA representations of the action as a global unit or as a set of elementary motor components? After outlining a model of the motor hierarchy, we conclude that the best candidate for SRA is intentions in action, defined as the motor plans of the dynamic sequence of movements. We shed new light on SRA by highlighting the causal efficacy of intentions in action. This in turn explains phenomena such as inhibition of imitation.

Much research has been carried out to understand how human brains make sense of another agent in motion. Current views based on human adult and monkey studies assume a matching process in the motor system biased toward actions performed by conspecifics and present in the observer's motor repertoire. However, little is known about the neural correlates of action cognition in early ontogeny. In this study, we examined the processes involved in the observation of full body movements in 4-month-old infants using functional near-infrared spectroscopy to measure localized brain activation. In a 2 × 2 design, infants watched human or robotic figures moving in a smooth, familiar human-like manner, or in a rigid, unfamiliar robot-like manner. We found that infant premotor cortex responded more strongly to observe robot-like motion compared with human-like motion. Contrary to current views, this suggests that the infant motor system is flexibly engaged by novel movement patterns. Moreover, temporal cortex responses indicate that infants integrate information about form and motion during action observation. The response patterns obtained in premotor and temporal cortices during action observation in these young infants are very similar to those reported for adults. These findings thus suggest that the brain processes involved in the analysis of an agent in motion in adults become functionally specialized very early in human development.

It has been postulated that when people engage in joint actions they form internal representations not only of their part of the joint task but of their co-actors' parts of the task as well. However, empirical evidence for this claim is scarce. By means of high-density electroencephalography, this study investigated whether one represents and simulates the action of an interaction partner when planning to perform a joint action. The results showed that joint action planning compared with individual action planning resulted in amplitude modulations of the frontal P3a and parietal P3b event-related potentials, which are associated with stimulus classification, updating of representations, and decision-making. Moreover, there was evidence for anticipatory motor simulation of the partner's action in the amplitude and peak latency of the late, motor part of the Contingent Negative Variation, which was correlated with joint action performance. Our results provide evidence that when people engage in joint tasks, they represent in advance each other's actions in order to facilitate coordination.

Traditionally, communication has been defined as the intentional exchange of symbolic information between individuals. In contrast, the mirror system provides a basis for nonsymbolic and nonintentional information exchange between individuals. We believe that understanding the role of the mirror system in joint action has the potential to serve as a bridge between these two domains. The present study investigates one crucial component of joint action: the ability to represent others' potential actions in the same way as one's own in the absence of perceptual evidence. In two experiments a joint spatial numerical association of response codes (SNARC) effect is demonstrated, providing further evidence that individuals form functionally equivalent representations of their own and others' potential actions. It is shown that numerical (symbolic) stimuli that are mapped onto a spatially arranged internal representation (a mental number line) can activate a co-represented action in the same way as spatial stimuli. This generalizes previous results on co-representation.We discuss the role of the mirror system in co-representation as a basis for shared intentionality and communication.