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.
Neuroimaging studies with adults have begun to reveal the neural bases of empathy; however, this research has focused on empathy for physical pain, rather than empathy for negative social experiences. Moreover, this work has not examined adolescents who may frequently witness and empathize with others who experience negative social experiences like peer rejection. Here, we examined neural activity among early adolescents observing social exclusion compared to observing inclusion, and how this activity related to both trait empathy and subsequent prosocial behavior. Participants were scanned while they observed an individual whom they believed was being socially excluded. At least one day prior to the scan they reported their trait empathy, and following the scan they wrote emails to the excluded victim that were rated for prosocial behavior (e.g., helping, comforting). Observing exclusion compared to inclusion activated regions involved in mentalizing (i.e., dorsomedial prefrontal cortex; DMPFC), particularly among highly empathic individuals. Additionally, individuals who displayed more activity in affective, pain-related regions during observed exclusion compared to inclusion subsequently wrote more prosocial emails to excluded victims. Overall findings suggest that when early adolescents witness social exclusion in their daily lives, some may actually ‘feel the pain’ of the victims and act more prosocially toward them as a result.
adolescence; empathy; peer rejection; social exclusion; functional magnetic resonance imaging
This study examined neural activity with event-related potentials (ERPs) in middle childhood during a computer-simulated ball-toss game, Cyberball. Experiencing fair play initially, children were ultimately excluded by the other players. We focused specifically on “not my turn” events within fair play and rejection events within social exclusion. Dense-array ERPs revealed that rejection events are perceived rapidly. Condition differences (“not my turn” vs. rejection) were evident in a posterior ERP peaking at 420 ms consistent, with a larger P3 effect for rejection events indicating that in middle childhood rejection events are differentiated in < 500 ms. Condition differences were evident for slow-wave activity (500–900 ms) in the medial frontal cortical region and the posterior occipital-parietal region, with rejection events more negative frontally and more positive posteriorly. Distress from the rejection experience was associated with a more negative frontal slow wave and a larger late positive slow wave, but only for rejection events. Source modeling with Geosouce software suggested that slow wave neural activity in cortical regions previously identified in functional imaging studies of ostracism, including subgenual cortex, ventral anterior cingulate cortex and insula was greater for rejection events vs. “not my turn” events.
Social exclusion; Social rejection; Middle childhood; Event-related potentials (ERPs); Source modeling
How people judge something to be morally right or wrong is a fundamental question of both the sciences and the humanities. Here we aim to identify the neural processes that underlie the specific conclusion that something is morally wrong. To do this, we introduce a novel distinction between “moral deliberation,” or the weighing of moral considerations, and the formation of a “moral verdict,” or the commitment to one moral conclusion. We predict and identify hemodynamic activity in the bilateral anterior insula and basal ganglia that correlates with committing to the moral verdict “this is morally wrong” as opposed to “this is morally not wrong,” a finding that is consistent with research from economic decision-making. Using comparisons of deliberation-locked vs. verdict-locked analyses, we also demonstrate that hemodynamic activity in high-level cortical regions previously implicated in morality—including the ventromedial prefrontal cortex, posterior cingulate, and temporoparietal junction—correlates primarily with moral deliberation as opposed to moral verdicts. These findings provide new insights into what types of processes comprise the enterprise of moral judgment, and in doing so point to a framework for resolving why some clinical patients, including psychopaths, may have intact moral judgment but impaired moral behavior.
Morality; Judgment; Anterior insula; Ventromedial prefrontal cortex
Positive behavioral responses to attractive faces have led neuroscientists to investigate underlying neural mechanisms in a ‘reward circuit’ that includes brain regions innervated by dopamine pathways. Using male faces ranging from attractive to extremely unattractive, disfigured ones, this study is the first to demonstrate heightened responses to both rewarding and aversive faces in numerous areas of this putative reward circuit. Parametric analyses employing orthogonal linear and nonlinear regressors revealed positive nonlinear effects in anterior cingulate cortex (ACC), lateral orbitofrontal cortex (LOFC), striatum (nucleus accumbens (NAC), caudate, putamen), and ventral tegmental area (VTA), in addition to replicating previously documented linear effects in MOFC and LOFC and nonlinear effects in AMY and MOFC. The widespread nonlinear responses are consistent both with single cell recordings in animals showing responses to both rewarding and aversive stimuli and some human fMRI investigations of non-face stimuli. They indicate that the reward circuit does not process face valence with any simple dissociation of function across structures. Perceiver gender modulated some responses to our male faces: women showed stronger linear effects, and men showed stronger nonlinear effects, which may have functional implications. Our discovery of nonlinear responses to attractiveness throughout the reward circuit echoes the history of amygdala research: early work indicated a linear response to threatening stimuli, including faces; later work also revealed a nonlinear response with heightened activation to affectively salient stimuli regardless of valence. The challenge remains to determine how such dual coding influences feelings, like pleasure and pain, and guides goal-related behavioral responses, like approach and avoidance.
facial attractiveness; fMRI; reward circuit
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 Theory of Mind regions activated less in participants with autism relative to control participants. In the autism group, an independent psychometric assessment of Theory of Mind 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 Theory of Mind in autism, implicating the underconnectivity between frontal regions and more posterior areas.
autism; mentalizing; Theory of Mind (ToM); mental state; fMRI; underconnectivity
Family assistance is an important aspect of family relationships for adolescents across many cultures and contexts. Motivations to help family members may be driven by both cultural factors and early family experiences. Here, we used functional magnetic resonance imaging to examine (1) cultural differences in neural reward activity among White and Latino youth during online experiences of family assistance and (2) how prior family experiences related to neural reward activity when helping the family. Participants were scanned as they made decisions to contribute money to their family and themselves. Latino and White participants showed similar behavioral levels of helping but distinct patterns of neural activity within the mesolimbic reward system. Whereas Latino participants showed more reward activity when contributing to their family, White participants showed more reward activity when gaining cash for themselves. In addition, participants who felt more identified with their family and who derived greater fulfillment from helping their family two years prior to the scan showed increased reward system activation when contributing to their family. These results suggest that family assistance may be guided, in part, by the personal rewards one attains from that assistance, and that this sense of reward may be modulated by cultural influences and prior family experiences.
Family assistance; Culture; fMRI; Reward; Social identity
Faces are a developmentally primary and critically important source of social information, and they are processed differently from most other visual percepts. Studies of brain electrophysiology reveal a face-sensitive component, the N170, which is typically enhanced to faces relative to other stimuli. Research in social disabilities suggests that an atypical N170 response in this population may stem from decreased developmental exposure to faces secondary to reduced social interest. Here we examined the relationship between neural responses to faces and social personality characteristics in a normative sample. Participants were pre-screened to identify individuals scoring high on extraversion or introversion. Both groups were presented upright and inverted face stimuli. An inversion effect, a marker of expertise for faces, was observed in people with high extraversion but not in those with high introversion. These findings suggest that, within typically developing populations, social attitudes are reflected in the neural correlates of face perception.
Personality; extraversion; social motivation; N170; event-related potential (ERP / EEG); face perception
The present study aimed at identifying dysfunctions in brain networks that may underlie disturbed empathic behavior in autism spectrum disorders (ASD). During functional magnetic resonance imaging, subjects were asked to identify the emotional state observed in a facial stimulus (other-task) or to evaluate their own emotional response (self-task). Behaviorally, ASD subjects performed equally to the control group during the other-task, but showed less emotionally congruent responses in the self-task. Activations in brain regions related to theory of mind were observed in both groups. Activations of the medial prefrontal cortex (MPFC) were located in dorsal subregions in ASD subjects and in ventral areas in control subjects. During the self-task, ASD subjects activated an additional network of frontal and inferior temporal areas. Frontal areas previously associated with the human mirror system were activated in both tasks in control subjects, while ASD subjects recruited these areas during the self-task only. Activations in the ventral MPFC may provide the basis for one's “emotional bond” with other persons’ emotions. Such atypical patterns of activation may underlie disturbed empathy in individuals with ASD. Subjects with ASD may use an atypical cognitive strategy to gain access to their own emotional state in response to other people's emotions.
Emotion; Medial prefrontal cortex; Neuroimaging; Self; Theory of mind; Autism
This study examined the neural substrates of facial familiarity and person-knowledge. Based on current neural models of face perception, it was hypothesized that distinct extended networks of brain regions differentiate the perception of (a) novel faces, (b) novel faces associated with person-knowledge, (c) perceptually familiar faces and (d) familiar faces for which person-knowledge was learned. To test this hypothesis, we conducted an event-related fMRI experiment during which participants viewed faces experimentally manipulated to represent these different levels of familiarity. Results confirmed that distinct networks of brain regions, particularly the medial prefrontal cortex (MPFC), underlie the perception of faces for which person-knowledge is available.