Behavioral data supports the commonsense view that babies elicit different responses than adults do. Behavioral research also has supported the babyface overgeneralization hypothesis that the adaptive value of responding appropriately to babies produces a tendency for these responses to be over-generalized to adults whose facial structure resembles babies. Here we show a neural substrate for responses to babies and babyface overgeneralization in the amygdala and the fusiform face area (FFA). Both regions showed greater percentage BOLD signal change compared with fixation when viewing faces of babies or babyfaced men than maturefaced men. Viewing the first two categories also yielded greater effective connectivity between the two regions. Facial qualities previously shown to elicit strong neural activation could not account for the effects. Babyfaced men were distinguished only by their resemblance to babies. The preparedness to respond to infantile facial qualities generalizes to babyfaced men in perceivers’ neural responses just as it does in their behavioral reactions.
Depressed mothers show negatively biased responses to their infants’ emotional bids, perhaps due to faulty processing of infant cues. This study is the first to examine depression-related differences in mothers’ neural response to their own infant’s emotion faces, considering both effects of perinatal depression history and current depressive symptoms. Primiparous mothers (n = 22), half of whom had a history of major depressive episodes (with one episode occurring during pregnancy and/or postpartum), were exposed to images of their own and unfamiliar infants’ joy and distress faces during functional neuroimaging. Group differences (depression vs. no-depression) and continuous effects of current depressive symptoms were tested in relation to neural response to own infant emotion faces. Compared to mothers with no psychiatric diagnoses, those with depression showed blunted responses to their own infant’s distress faces in the dorsal anterior cingulate cortex. Mothers with higher levels of current symptomatology showed reduced responses to their own infant’s joy faces in the orbital-frontal cortex and insula. Current symptomatology also predicted lower responses to own infant joy–distress in left-sided prefrontal and insula/striatal regions. These deficits in self-regulatory and motivational response circuits may help explain parenting difficulties in depressed mothers.
maternal depression; infant; faces; emotion; fMRI
Although previous behavioral studies have shown that schizophrenia patients have impaired theory of mind (ToM), the neural mechanisms associated with this impairment are poorly understood. This study aimed to identify the neural mechanisms of ToM in schizophrenia using functional magnetic resonance imaging (fMRI) with a Belief Attribution Task.
In the scanner, 12 schizophrenia patients and 13 healthy control subjects performed the Belief Attribution Task with 3 conditions: a false belief condition, a false photograph condition, and a simple reading condition.
For the false belief vs. simple reading conditions, schizophrenia patients showed reduced neural activation in areas including the temporo-parietal junction (TPJ) and medial prefrontal cortex (MPFC) compared with controls. Further, during the false belief vs. false photograph conditions we observed increased activations in the TPJ and the MPFC in healthy controls, but not in schizophrenia patients. For the false photograph vs. simple reading condition, both groups showed comparable neural activations.
Schizophrenia patients showed reduced task-related activation in the TPJ and the MPFC during the false belief condition compared with controls, but not for the false photograph condition. This pattern suggests that reduced activation in these regions is associated with, and specific to, impaired ToM in schizophrenia.
theory of mind; belief attribution; schizophrenia; fMRI; social cognition
The impact of emotions on gaze-oriented attention was investigated in non-anxious participants. A neutral face cue with straight gaze was presented, which then averted its gaze to the side while remaining neutral or expressing an emotion (fear/surprise in Exp.1 and anger/happiness in Exp.2). Localization of a subsequent target was faster at the gazed-at location (congruent condition) than at the non-gazed-at location (incongruent condition). This Gaze-Orienting Effect (GOE) was enhanced for fear, surprise, and anger, compared to neutral expressions which did not differ from happy expressions. In addition, Event Related Potentials (ERPs) to the target showed a congruency effect on P1 for fear and surprise and a left lateralized congruency effect on P1 for happy faces, suggesting that target visual processing was also influenced by attention to gaze and emotions. Finally, at cue presentation, early postero-lateral (Early Directing Attention Negativity (EDAN)) and later antero-lateral (Anterior Directing Attention Negativity (ADAN)) attention-related ERP components were observed, reflecting, respectively, the shift of attention and its holding at gazed-at locations. These two components were not modulated by emotions. Together, these findings show that the processing of social signals such as gaze and facial expression interact rather late and in a complex manner to modulate spatial attention.
PMID: 24047232 CAMSID: cams3897
Gaze orienting; Attention; ERPs; Emotions
Emotions elicited by interpersonal versus non-interpersonal experiences have different effects on neurobiological functioning in both animals and humans. However, the extent to which the brain circuits underlying interpersonal and non-interpersonal emotions are distinct still remains unclear. The goal of our study was to assess whether different neural circuits are implicated in the processing of arousal and valence of interpersonal versus non-interpersonal emotions. During functional magnetic resonance imaging, participants imagined themselves in emotion-eliciting interpersonal or non-interpersonal situations and then rated the arousal and valence of emotions they experienced. We identified (a) separate neural circuits that are implicated in the arousal and valence dimensions of interpersonal versus non-interpersonal emotions, (b) circuits that are implicated in arousal and valence for both types of emotion, and (c) circuits that are responsive to the type of emotion, regardless of the valence or arousal level of the emotion. We found extensive recruitment of limbic (for arousal) and temporal-parietal (for valence) systems associated with processing of specifically interpersonal emotions compared to non-interpersonal ones. The neural bases of interpersonal and non-interpersonal emotions may, therefore, be largely distinct.
emotion; interpersonal; social; circumplex model of affect; fMRI
Prediction error, the difference between an expected and actual outcome, serves as a learning signal that interacts with reward and punishment value to direct future behavior during reinforcement learning. We hypothesized that similar learning and valuation signals may underlie social expectancy violations. Here, we explore the neural correlates of social expectancy violation signals along the universal person-perception dimensions of trait warmth and competence. In this context, social learning may result from expectancy violations that occur when a target is inconsistent with an a priori schema. Expectancy violation may activate neural regions normally implicated in prediction error and valuation during appetitive and aversive conditioning. Using fMRI, we first gave perceivers warmth or competence behavioral information. Participants then saw pictures of people responsible for the behavior; they represented social groups either inconsistent (rated low on either warmth or competence) or consistent (rated high on either warmth or competence) with the behavior information. Warmth and competence expectancy violations activate striatal regions and frontal cortex respectively, areas that represent evaluative and prediction-error signals. These findings suggest that regions underlying reinforcement learning may be engaged in warmth and competence social expectancy violation, and illustrate the neural overlap between neuroeconomics and social neuroscience.
stereotype content model; trait attribution; social expectancy violation; trait warmth and competence
Anxiety plays an important role in social behavior. For instance, high-anxious individuals are more likely to avoid such social interactions as communicating with strangers. In this study, we investigate the impact of anxiety on social decision-making. The classic Ultimatum Game (UG) paradigm was utilized in concert with skin conductance recording. Behavioral results reveal that when playing as responders, high-trait anxiety (HTA) participants with lower levels of self-esteem, as well as low-trait anxiety (LTA) participants with higher levels of impulsivity, were more likely to accept human-proposed inequitable offers. In addition, HTA participants rejected more computer-proposed inequitable offers than did LTA participants. Moreover, the skin conductance response to inequitable offers was correlated with levels of anxiety in the HTA group, but not in the LTA group. In conclusion, people differing in levels of anxiety showed distinct behavior patterns and autonomic neural responses during social decision-making, while levels of self-esteem, impulsivity and depression might be additional moderating factors. These findings contextualize high-anxious people’s avoidance tendency in social interaction.
anxiety; social decision-making; Ultimatum Game (UG); fairness; skin conductance responses (SCRs); self-esteem; impulsivity
Recent work suggests the existence of a specialized neural system underlying social processing that may be relatively spared with age, unlike pervasive aging-related decline occurring in many cognitive domains. We investigated how neural mechanisms underlying social evaluation are engaged with age, and how age-related changes to socioemotional goals affect recruitment of regions within this network. In a functional MRI study, fifteen young and fifteen older adults formed behavior-based impressions of individuals. They also responded to a prompt that was interpersonally meaningful, social but interpersonally irrelevant, or non-social. Both age groups engaged regions implicated in mentalizing and impression formation when making social relative to non-social evaluations, including dorsal and ventral medial prefrontal cortices, precuneus, and temporoparietal junction. Older adults had increased activation over young in right temporal pole when making social relative to non-social evaluations, suggesting reliance on past experiences when evaluating others. Young had greater activation than old in posterior cingulate gyrus when making interpersonally irrelevant, compared to interpersonally meaningful, evaluations, potentially reflecting enhanced valuation of this information. The findings demonstrate the age-related preservation of the neural correlates underlying social evaluation, and suggest that functioning in these regions might be mediated by age-related changes in socioemotional goals.
impression formation; aging; fMRI; dorsomedial prefrontal cortex; posterior cingulate gyrus
A foundational aspect of early social-emotional development is the ability to detect and respond to the actions of others who are coordinating their behavior with that of the self. Behavioral work in this area has found that infants show particular preferences for adults who are imitating them rather than adults who are carrying out noncontingent or mismatching actions. Here we explore the neural processes related to this tendency of infants to prefer others who act like the self. EEG was recorded from 14-month-olds while they were observing actions which either matched or mismatched the action the infant had just executed. Desynchronization of the EEG mu rhythm was greater when infants observed an action that matched their own most recently executed action. This effect was strongest immediately prior to the culmination of the goal of the observed action, which is consistent with recent ideas about the predictive nature of brain responses during action observation.
EEG; mu rhythm; imitation; perception-action; infant
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, 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 prefrontal cortex 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 prefrontal cortex (BA 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 prefrontal cortex contributes to this source memory benefit. This evidence expands the purported role that the medial prefrontal cortex plays in self-referencing.
Medial prefrontal cortex; Self-reference; Source memory
Williams syndrome (WS) is a genetic condition with a distinctive social phenotype characterized by excessive sociability, accompanied by a relative proficiency in face recognition, despite severe deficits in visuospatial domain of cognition. This consistent phenotypic characteristic and the relative homogeneity of the WS genotype make WS a compelling human model for examining the genotype-phenotype relations, especially with respect to social behavior. Following up on a recent report suggesting that individuals with WS do not show race bias and racial stereotyping, this study was designed to investigate the neural correlates of the perception of faces from different races, in individuals with WS as compared to typically developing (TD) controls. Caucasian WS and TD participants performed a gender identification task with own-race (White) and other-race (Black) faces while event-related potentials (ERPs) were recorded. In line with previous studies with TD participants, other-race faces elicited larger amplitudes ERPs within the first 200 ms following the face onset, in WS and TD participants alike. These results suggest that, just like their TD counterparts, individuals with WS differentially processed faces of own- vs. other-race, at relatively early stages of processing, starting as early as 115 ms after the face onset. Overall, these results indicate that neural processing of faces in individuals with WS is moderated by race at early perceptual stages, calling for a reconsideration of the previous claim that they are uniquely insensitive to race.
Williams syndrome; the other-race effect; event-related potentials; race bias
Mere familiarization with a stimulus increases liking for it or similar stimuli (‘mere exposure’ effects) as well as perceptual fluency, indexed by the speed and accuracy of categorizing it or similar stimuli (‘priming’ effects). Candidate mechanisms proposed to explain mere exposure effects include both increased positive affect associated with greater perceptual fluency, and also reduced negative affect associated with diminished apprehensiveness of novel stimuli. Although these two mechanisms are not mutually exclusive, it is difficult for behavioral measures to disentangle them, since increased liking or other indices of greater positive affect toward exposed stimuli could result from increases in positive feelings or decreases in negative feelings or both. The present study sought to clarify this issue by building on research showing a dissociation at the neural level in which the lateral orbital frontal cortex (LOFC) is activated more by negatively valenced than by neutral or positively valenced stimuli, with the reverse effect for medial orbital frontal cortex (MOFC). Supporting the reduced apprehensiveness hypothesis, we found lower LOFC activation to familiarized faces and objects (repetition suppression). We did not find evidence to support the positive affect hypothesis in increased activation to familiarized stimuli in MOFC or in other parts of the reward circuit that respond more to positively valenced stimuli (repetiton enhancement), although enhancement effects were shown in some regions.
Emotion research is guided both by the view that emotions are points in a dimensional space, such as valence or approach–withdrawal, and by the view that emotions are discrete categories. We determined whether effective connectivity of amygdala with medial orbitofrontal cortex (MOFC) and lateral orbitofrontal cortex (LOFC) differentiates the perception of emotion faces in a manner consistent with the dimensional and/or categorical view. Greater effective connectivity from left MOFC to amygdala differentiated positive and neutral expressions from negatively valenced angry, disgust, and fear expressions. Greater effective connectivity from right LOFC to amygdala differentiated emotion expressions conducive to perceiver approach (happy, neutral, and fear) from angry expressions that elicit perceiver withdrawal. Finally, consistent with the categorical view, there were unique patterns of connectivity in response to fear, anger, and disgust, although not in response to happy expressions, which did not differ from neutral ones.
Amygdala; OFC; Connectivity; Face; Emotion perception
Some older adults without neurological disease exhibit impaired decision-making in risky, non-transparent situations, like the Iowa Gambling Task (IGT). The prefrontal cortices are particularly vulnerable to age-related decline, and numerous studies implicate the ventromedial prefrontal cortex (VMPFC) in successful IGT performance. However, the relationship between IGT performance and VMPFC function in older adults has not yet been tested using fMRI. In the present study older adults with seemingly no cognitive impairments performed the IGT and a non-gambling control task during fMRI. Group analyses indicate that in these older adults, regardless of IGT performance level, a right VMPFC sub-region is activated during the IGT, while successful IGT performance is correlated with left VMPFC activation, suggesting that bilateral VMPFC during risky, non-transparent situations may contribute to successful decision-making in older adults. Individual subject analyses reveal substantial variation regarding the extent and location of VMPFC activation during the IGT, a finding not captured in the group analysis: there is no correlation between IGT performance and extent of activation in the right VMPFC, although there is such a correlation between left VMPFC activation and IGT performance.
Successful human interaction is based on correct recognition, interpretation and appropriate reaction to facial affect. In depression, social skill deficits are among the most restraining symptoms leading to social withdrawal, thereby aggravating social isolation and depressive affect. Dysfunctional approach and withdrawal tendencies towards emotional stimuli have been documented but the investigation of their neural underpinnings has received limited attention. We performed an fMRI study including 15 depressive patients and 15 matched healthy controls. All subjects performed two tasks, an implicit joystick task as well as an explicit rating task both using happy, neutral, and angry facial expressions.
Behavioral data analysis indicated a significant group effect, with depressed patients showing more withdrawal than controls. Analysis of the functional data revealed significant group effects for both tasks. Amongst other regions, we observed significant group differences in amygdala activation with patients showing less response particularly during approach of happy faces. Additionally, significant correlations of amygdala activation with psychopathology emerged, suggesting that more pronounced symptoms are accompanied by stronger decreases of amygdala activation.
Hence, our results demonstrate that depressed patients show dysfunctional social approach and withdrawal behavior, which in turn may aggravate the disorder by negative social interactions contributing to isolation and reinforcing cognitive biases.
depression; approach; withdrawal; emotion; amygdala; fMRI
The social motivation hypothesis posits that aberrant neural response to human faces in autism is attributable to atypical social development and consequently reduced exposure to faces. The specificity of deficits in neural specialization remains unclear, and alternative theories suggest generalized processing difficulties. The current study contrasted neural specialization for social information versus non-social information in 36 individuals with autism and 18 typically developing individuals matched for age, race, sex, handedness, and cognitive ability. Event-related potentials elicited by faces, inverted faces, houses, letters, and pseudoletters were recorded. Groups were compared on an electrophysiological marker of neural specialization (N170), as well as behavioral performance on standardized measures of face recognition and word reading/decoding. Consistent with prior results, individuals with autism displayed slowed face processing and decreased sensitivity to face inversion; however, they showed comparable brain responses to letters, which were associated with behavioral performance in both groups. Results suggest that individuals with autism display atypical neural specialization for social information but intact specialization for non-social information. They concord with the notion of specific dysfunction in social brain systems rather than non-specific information processing difficulties in autism.
Perceptual expertise; N170; event-related potential (ERP/EEG); face perception; autism spectrum disorder
The ability to make accurate judgments about the mental states of others, sometimes referred to as theory of mind (ToM), is often impaired following traumatic brain injury (TBI), and this deficit may contribute to problems with interpersonal relationships. The present study used an animated social attribution task (SAT) with functional magnetic resonance imaging (fMRI) to examine structures mediating ToM in adolescents with moderate to severe TBI. The study design also included a comparison group of matched, typically developing (TD) adolescents. The TD group exhibited activation within a number of areas that are thought to be relevant to ToM, including the medial prefrontal and anterior cingulate cortex, fusiform gyrus, and posterior temporal and parietal areas. The TBI subjects had significant activation within many of these same areas, but their activation was generally more intense and excluded the medial prefrontal cortex. Exploratory regression analyses indicated a negative relation between ToM-related activation and measures of white matter integrity derived from diffusion tensor imaging, while there was also a positive relation between activation and lesion volume. These findings are consistent with alterations in the level and pattern of brain activation that may be due to the combined influence of diffuse axonal injury and focal lesions.
Traumatic brain injury; fMRI; Social cognition; Adolescents; Diffusion tensor imaging
Individuals who engage in corrupt and immoral behavior are in some ways similar to psychopaths. Normal people refrain from engaging in such behaviors because they tie together the moral value of society and the risk for punishment when they violate social rules. What is it, then, that allows these immoral individuals to behave in this manner, and in some situations to even prosper? When there is a dysfunction of somatic markers, specific disadvantageous impairments in decision-making arise, for example in moral judgment, but paradoxically, under some circumstances, the damage can cause the patient to make optimal financial investment decisions. Interestingly, individuals with psychopathy, a personality disorder, share many of these same behavioral characteristics as those seen in VMPFC and amygdala lesion patients, suggesting that defective somatic markers may serve as a neural framework for explaining immoral and corrupt behaviors. While these sociopathic behaviors of sometimes famous and powerful individuals have long been discussed primarily within the realm of social science and psychology, here we offer a neurocognitive perspective on possible neural roots for immoral and corrupt behaviors.
somatic marker hypothesis; psychopathy; corruption; immorality; decision-making
Self-construals are different between Western and East Asian cultures in that the Western self emphasizes more on self-focused attention whereas the East Asian self stresses more on the fundamental social connections between people. To investigate whether such cultural difference in self-related processing extends to face recognition, we recorded event-related potentials from British and Chinese subjects while they judged head orientations of their own face or a familiar face in visual displays. For the British, the own-face induced faster responses and a larger negative activity at 280-340 ms over the frontal-central area (N2) relative to the familiar face. In contrast, the Chinese showed weakened self-advantage in behavioral responses and reduced anterior N2 amplitude to the own-face compared with the familiar face. Our findings suggest that enhanced social salience of one’s own face results in different neurocognitive processes of self-recognition in Western and Chinese cultures.
culture; event-related potential; face; self
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 250-550 ms (N300/N400 effects), reflecting the integration of accumulating sex-category knowledge into a coherent sex-category interpretation. Additionally, the lateralized readiness potential (LRP) 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.
person perception; action; face perception; social categorization; motor processes; ERPs
The amygdala plays a critical role in orienting gaze and attention to socially salient stimuli. Previous work has demonstrated that SM a patient with rare bilateral amygdala lesions, fails to fixate and make use of information from the eyes in faces. Amygdala dysfunction has also been implicated as a contributing factor in autism spectrum disorders (ASD), consistent with some reports of reduced eye fixations in ASD. Yet, detailed comparisons between ASD and patients with amygdala lesions have not been undertaken. Here we carried out such a comparison, using eye tracking to complex social scenes that contained faces. We presented participants with three task conditions. In the Neutral task, participants had to determine what kind of room the scene took place in. In the Describe task, participants described the scene. In the Social Attention task, participants inferred where people in the scene were directing their attention. SM spent less time looking at the eyes and much more time looking at the mouths than control subjects, consistent with earlier findings. There was also a trend for the ASD group to spend less time on the eyes, although this depended on the particular image and task. Whereas controls and SM looked more at the eyes when the task required social attention, the ASD group did not. This pattern of impairments suggests that SM looks less at the eyes because of a failure in stimulus-driven attention to social features, whereas individuals with ASD look less at the eyes because they are generally insensitive to socially relevant information and fail to modulate attention as a function of task demands. We conclude that the source of the social attention impairment in ASD may arise upstream from the amygdala, rather than in the amygdala itself.
Social attention; Amygdala; Autism; Scene perception; Gaze selection
Previous research suggests hypoactivity in response to the visual perception of faces in the fusiform gyri and amygdalae of individuals with autism. However, critical questions remain regarding the mechanisms underlying these findings. In particular, to what degree is the hypoactivation accounted for by known differences in the visual scanpaths exhibited by individuals with and without autism in response to faces? Here, using functional magnetic resonance imaging (fMRI), we report “normalization” of activity in the right fusiform gyrus, but not the amygdalae, when individuals with autism were compelled to perform visual scanpaths that involved fixating upon the eyes of a fearful face. These findings hold important implications for our understanding of social brain dysfunction in autism, theories of the role of the fusiform gyri in face processing, and the design of more effective interventions for autism.
Autism; Face Perception; Functional Magnetic Resonance Imaging; Fusiform Gyrus; Amygdala
Emotion regulation is a critical aspect of children's social development, yet few studies have examined the brain mechanisms involved in the development of emotion regulation. Theoretical accounts have conceptualized emotion regulation as relying upon prefrontal control of limbic regions, specifying the anterior cingulate cortex (ACC) as a key brain region for the regulation of emotion. Functional magnetic resonance imaging (fMRI) in 5- to 11-year-olds during emotion regulation and processing of emotionally expressive faces revealed that older children preferentially recruited the more dorsal “cognitive” areas of the ACC, while younger children preferentially engaged the more ventral “emotional” areas. Additionally, children with more fearful temperaments exhibited more ventral ACC activity while less fearful children exhibited increased activity in the dorsal ACC. These findings provide insight into a potential neurobiological mechanism underlying well-documented behavioral and cognitive changes from more emotional to more cognitive regulatory strategies with increasing age, as well as individual differences in this developmental process as a function of temperament. Our results hold important implications for our understanding of normal development and should also help to inform our understanding and management of emotional disorders.
Emotion Regulation; Development; fMRI; Anterior Cingulate; Temperament
Relational aggression describes a type of aggression that aims to hurt others through relationships and includes behaviors such as gossip and ostracism. This type of aggression is very common among adolescent girls; and in its more intense forms has been linked with poor psychosocial outcomes, including depression and suicide. In the present study we investigated whether individual differences in sensitivity to relational aggression among adolescent girls predicted recruitment of neural networks associated with executive function and cognitive control. Neural response was measured using functional magnetic resonance imaging (fMRI) during an affect recognition task that included unfamiliar peer faces. We found that relatively fewer reports of being victimized by relational aggression was associated increased recruitment of bilateral dorsolateral prefrontal cortices as well as anterior and posterior cingulate cortices in response to the affect recognition task, as well as with greater competence on behavioral measures of executive function. Our results suggest that girls who are able to recruit specific frontal networks to improve cognitive and executive control are relatively less sensitive to relational aggression.