Males have been suggested to have advantages over females in reactions to child facial resemblance, which reflects the evolutionary pressure on males to solve the adaptive paternal uncertainty problem and to identify biological offspring. However, previous studies showed inconsistent results and the male advantage in child facial resemblance perception, as a kin detection mechanism, is still unclear. Here we investigated the behavioral and brain mechanisms underlying the self-resembling faces processing and how it interacts with sex and age using ERP technique. The results showed a stable male advantage in self-resembling child faces processing, such that males have higher detectability to self-resembling child faces than females. For ERP results, males showed smaller N2 and larger LPC amplitudes for self-resembling child faces, which may reflect face-matching and self-referential processing in kin detection, respectively. Further source analysis showed that the N2 and LPC components were originated from the anterior cingulate cortex and medial frontal gyrus, respectively. Our results support the male advantage in self-resembling child detection and further indicate that such distinctions can be found in both early and late processing stages in the brain at different regions.
Kin recognition; Facial resemblance; Parental uncertainty; Paternity cue
The decision to shoot engages executive control processes that can be biased by cultural stereotypes and perceived threat. The neural locus of the decision to shoot is likely to be found in the anterior cingulate cortex (ACC) where cognition and affect converge. Male military cadets at Norwich University (N=37) performed a weapon identification task in which they made rapid decisions to shoot when images of guns appeared briefly on a computer screen. Reaction times, error rates, and EEG activity were recorded. Cadets reacted more quickly and accurately when guns were primed by images of middle-eastern males wearing traditional clothing. However, cadets also made more false positive errors when tools were primed by these images. Error-related negativity (ERN) was measured for each response. Deeper ERN’s were found in the medial-frontal cortex following false positive responses. Cadets who made fewer errors also produced deeper ERN’s, indicating stronger executive control. Pupil size was used to measure autonomic arousal related to perceived threat. Images of middle-eastern males in traditional clothing produced larger pupil sizes. An image of Osama bin Laden induced the largest pupil size, as would be predicted for the exemplar of Middle East terrorism. Cadets who showed greater increases in pupil size also made more false positive errors. Regression analyses were performed to evaluate predictions based on current models of perceived threat, stereotype activation, and cognitive control. Measures of pupil size (perceived threat) and ERN (cognitive control) explained significant proportions of the variance in false positive errors to middle-eastern males in traditional clothing, while measures of reaction time, signal detection response bias, and stimulus discriminability explained most of the remaining variance.
Weapon Bias; Stereotypes; Threat Perception; Event-Related Potentials; Pupil Size; Anterior Cingulate Cortex
Looming stimuli are processed as threatening and activate basic neural defense systems. However, it is unclear how animacy information modulates this response. Participants (N = 25) viewed threatening or neutral images that were either animate (animals) or inanimate (objects) and which either approached (loomed) or receded from the participant. The amygdala was responsive to emotional, animacy and looming information (particularly to looming threats and looming animate stimuli). Periaqueductal gray was also sensitive to emotional information and particularly responsive to looming threats. The data are interpreted within category specific models of the amygdala and temporal cortex.
Amygdala; Animacy; Threat; Looming; Periaqueductal Gray
Reports of age-related changes to medial prefrontal cortex (mPFC) activity during socio-cognitive tasks have shown both age-equivalence and under recruitment. Emotion work illustrates selective mPFC response dependent on valence, such that negative emotional images evoke increased ventral mPFC activity for younger adults, while older adults recruit ventral mPFC more for positive material. By testing whether this differential age-related response toward valenced material is also present for the social task of forming impressions, we may begin to understand inconsistencies regarding when age differences are present vs. absent in the literature. Using fMRI, participants intentionally formed impressions of positive and negative face-behavior pairs in anticipation of a memory task. Extending previous findings to a social task, valence-based reversals were present in dorsal and ventral mPFC, and posterior cingulate cortex. Younger adults elicited increased activity when forming negative impressions, while older adults had more recruitment when forming positive impressions. This suggests an age-related shift toward emphasizing positive social information may be reflected in the recruitment of regions supporting forming impressions. Overall, the results indicate an age-related shift in neural response to socio-cognitive stimuli that is valence dependent rather than a general age-related reduction in activity, in part informing prior inconsistencies within the literature.
aging; medial prefrontal cortex; impression formation; valence
The importance of differentiating between social concepts when appraising actions (e.g. understanding behaviour as “critical” vs. “fault-finding”) and its contribution to vulnerability to major depressive disorder (MDD) is unknown. We predicted poor integration of differentiated conceptual knowledge when people with MDD appraise their social actions, contributing to their tendency to grossly overgeneralize self-blame (e.g. “I am unlikable rather than critical”). To test this hypothesis, we used a neuropsychological test measuring social conceptual differentiation and its relationship with emotional biases in a remitted MDD and a control group. During fMRI guilt- and indignation-evoking sentences were presented. As predicted, conceptual overgeneralization was associated with increased emotional intensity when appraising social actions. Interdependence of conceptual overgeneralization and negative emotional biases was stronger in MDD (reproducible in the subgroup without medication) and was associated with overgeneralized self-blame. This high conceptual-emotional interdependence was associated with functional disconnection between the right superior anterior temporal lobe (ATL) and right dorsolateral prefrontal cortex as well as a septal region across groups when experiencing guilt (SPM8). Strong coupling of conceptual information (ATL) with information about the context of actions and emotions (frontal-subcortical regions) is thus associated with appraisal being less dependent on conceptual overgeneralization, thereby protecting against excessive self-blame.
social concepts; moral emotions; overgeneralization; major depression; vulnerability; self-blame; information theory; differentiation; redundancy; emotional biases
The developmental origin of sex differences in adult brain function is poorly understood. Elucidating neural mechanisms underlying comparable cognitive functionality in both children and adults is required to address this gap. Humor appreciation represents a particularly relevant target for such developmental research because explanatory theories apply across the life span and underlying neurocircuitry shows sex differences in adults. As a positive mood state, humor is also of interest due to sex differences in rates of depression, a disorder afflicting twice as many women as men. In this study, we employed fMRI to investigate brain responses to funny versus positive (and neutral) video clips in 22 children ages 6 to 13 years, including 8 sibling pairs. Our data revealed increased activity to funny clips in bilateral temporo-occipital cortex, midbrain, and amygdala in girls. Conversely, we found heightened activation to positive clips in bilateral inferior parietal lobule, fusiform gyrus, inferior frontal gyrus, amygdala, and ventromedial prefrontal cortex in boys. Many of these effects persisted when looking at sibling-pairs only. We interpret such findings as reflecting the presence of early sex divergence in reward saliency / expectation and stimulus relevance attribution. These findings are discussed in the context of evolutionary and developmental theories of humor function.
Humor Appreciation; Sex Differences; Reward; Children; fMRI
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