Do surprised faces affect infants' attention toward novel objects?

Previous research has shown that expressions of fear have an effect on infants' object processing. This event-related potential study addresses the question whether surprised faces affect infants' brain responses to objects in a similar way, as both expressions share a crucial perceptual feature, wide-opened eyes. Three-month and 9-month-old infants were presented with surprised and neutral faces gazing toward objects. Following each face looking toward an object, the object was presented again without the face. Three-month-olds directed an increased attention to objects that were previously gaze cued by a surprised compared with neutral face as indicated by an enhanced negative central component. This replicates earlier findings using fearful compared with neutral faces as stimuli. Nine-month-olds did not show different responses to objects in both conditions. This suggests that surprised faces have the same effect as fearful faces on 3-month-olds', but not on 9-month-olds' object processing. The findings are discussed in terms of social cognitive and visuoperceptual development.     

Processing of facial expressions of same-race and other-race faces: distinct and shared neural underpinnings

People understand others’ emotions quickly from their facial expressions. However, facial expressions of ingroup and outgroup members may signal different social information and thus be mediated by distinct neural activities. We investigated whether there are distinct neuronal responses to fearful and happy expressions of same-race (SR) and other-race (OR) faces. We recorded electroencephalogram from Chinese adults when viewing an adaptor face (with fearful/neutral expressions in Experiment 1 but happy/neutral expressions in Experiment 2) and a target face (with fearful expressions in Experiment 1 but happy expressions in Experiment 2) presented in rapid succession. We found that both fearful and happy (vs neutral) adaptor faces increased the amplitude of a frontocentral positivity (P2). However, a fearful but not happy (vs neutral) adaptor face decreased the P2 amplitudes to target faces, and this repetition suppression (RS) effect occurred when adaptor and target faces were of the same race but not when of different races. RS was observed on two late parietal/central positive activities to fearful/happy target faces, which, however, occurred regardless of whether adaptor and target faces were of the same or different races. Our findings suggest that early affective processing of fearful expressions may engage distinct neural activities for SR and OR faces.     

Adult gaze influences infant attention and object processing: implications for cognitive neuroscience

Infants follow others' gaze toward external objects from early in ontogeny, but whether they use others' gaze in processing information about objects remains unknown. In Experiment 1, 4-month-old infants viewed a video presentation of an adult gazing toward one of two objects. When presented with the same objects alone a second time, infants looked reliably less at the object to which the adult had directly gazed (cued object). This suggests that the uncued object was perceived as more novel than the object previously cued by the adult's gaze. In Experiment 2, adult gaze was not directed towards any object. In this control experiment, infants looked at both objects equally in the test phase. These findings show that adult eye gaze biases infant visual attention and information processing. Implications of the paradigm for cognitive neuroscience are presented and the results are discussed in terms of neural structures and change over ontogeny.     

Gaze cues of isolated eyes facilitate the encoding and further processing of objects in 4-month-old infants

We investigated young infants’ object encoding and processing in response to isolated eye gaze cues on the neural and behavioral level. In two experiments, 4-month-old infants watched a pair of isolated eyes gazing towards or away from novel objects. Subsequently, the same objects were presented alone (i.e., without eyes). We measured event-related potentials (ERP) in response to object-directed and object-averted eye gaze as well as to the subsequently presented isolated objects. Using eye-tracking methods, we additionally measured infants’ looking behavior in reaction to the subsequently presented isolated objects. The ERP data revealed an enhanced slow wave positivity for object-directed eye gaze, indicating increased encoding of observed gaze cues. Regarding the objects, we found an enhanced Nc amplitude and increased looking times in response to previously uncued objects, indicating a novelty response on the neural and behavioral level. The results suggest that isolated eye gaze stimuli are sufficient to trigger object encoding and facilitate further object processing.     

Infants' attention is biased by emotional expressions and eye gaze direction

This study investigates infants' processing of emotional expressions in combination with referential eye gaze cues. In experiment 1, 7-month-old infants' neural responses to fearful and neutral faces, which were looking at a novel object, were assessed. Infants' attention, as indexed by the negative central component of the event-related potential, was enhanced when the adult gazed at the object with a fearful expression compared with a neutral expression. In experiment 2, no effect of emotion on amplitude of the negative central was found when the face directed eye gaze at the infant and away from the object. We conclude that by 7 months, infants use emotional expressions in triadic person-object-person contexts to detect threat in the environment.     

Eye gaze cueing facilitates neural processing of objects in 4-month-old infants

A major issue in developmental science is how infants use the direction of other's eye gaze to facilitate the processing of information. Four-month-old infants passively viewed images of an adult face gazing toward or away from objects. When presented with the objects a second time, infants showed differences in a slow wave event-related potential, indicating that uncued objects were perceived as less familiar than objects previously cued by the direction of gaze of another person. This result shows that the direction of eye gaze of another cannot only bias infant attention, but also lead to enhanced information processing of the objects concerned.     

Prediction errors to emotional expressions: the roles of the amygdala in social referencing

Social referencing paradigms in humans and observational learning paradigms in animals suggest that emotional expressions are important for communicating valence. It has been proposed that these expressions initiate stimulus-reinforcement learning. Relatively little is known about the role of emotional expressions in reinforcement learning, particularly in the context of social referencing. In this study, we examined object valence learning in the context of a social referencing paradigm. Participants viewed objects and faces that turned toward the objects and displayed a fearful, happy or neutral reaction to them, while judging the gender of these faces. Notably, amygdala activation was larger when the expressions following an object were less expected. Moreover, when asked, participants were both more likely to want to approach, and showed stronger amygdala responses to, objects associated with happy relative to objects associated with fearful expressions. This suggests that the amygdala plays two roles in social referencing: (i) initiating learning regarding the valence of an object as a function of prediction errors to expressions displayed toward this object and (ii) orchestrating an emotional response to the object when value judgments are being made regarding this object.     

The influence of personality on neural mechanisms of observational fear and reward learning

Fear and reward learning can occur through direct experience or observation. Both channels can enhance survival or create maladaptive behavior. We used fMRI to isolate neural mechanisms of observational fear and reward learning and investigate whether neural response varied according to individual differences in neuroticism and extraversion. Participants learned object-emotion associations by observing a woman respond with fearful (or neutral) and happy (or neutral) facial expressions to novel objects. The amygdala-hippocampal complex was active when learning the object-fear association, and the hippocampus was active when learning the object-happy association. After learning, objects were presented alone; amygdala activity was greater for the fear (vs. neutral) and happy (vs. neutral) associated object. Importantly, greater amygdala-hippocampal activity during fear (vs. neutral) learning predicted better recognition of learned objects on a subsequent memory test. Furthermore, personality modulated neural mechanisms of learning. Neuroticism positively correlated with neural activity in the amygdala and hippocampus during fear (vs. neutral) learning. Low extraversion/high introversion was related to faster behavioral predictions of the fearful and neutral expressions during fear learning. In addition, low extraversion/high introversion was related to greater amygdala activity during happy (vs. neutral) learning, happy (vs. neutral) object recognition, and faster reaction times for predicting happy and neutral expressions during reward learning. These findings suggest that neuroticism is associated with an increased sensitivity in the neural mechanism for fear learning which leads to enhanced encoding of fear associations, and that low extraversion/high introversion is related to enhanced conditionability for both fear and reward learning.     

Event-related potentials reveal temporal staging of dynamic facial expression and gaze shift effects on attentional orienting

Abstract

Multiple sources of information from the face guide attention during social interaction. The present study modified the Posner cueing paradigm to investigate how dynamic changes in emotional expression and eye gaze in faces affect the neural processing of subsequent target stimuli. Event-related potentials (ERPs) were recorded while participants viewed centrally presented face displays in which gaze direction (left, direct, right) and facial expression (fearful, neutral) covaried in a fully crossed design. Gaze direction was not predictive of peripheral target location. ERP analysis revealed several sequential effects, including: (1) an early enhancement of target processing following fearful faces (P1); (2) an interaction between expression and gaze (N1), with enhanced target processing following fearful faces with rightward gaze; and (3) an interaction between gaze and target location (P3), with enhanced processing for invalidly cued left visual field targets. Behaviorally, participants responded faster to targets following fearful faces and targets presented in the right visual field, in concordance with the P1 and N1 effects, respectively. The findings indicate that two nonverbal social cues—facial expression and gaze direction—modulate attentional orienting across different temporal stages of processing. Results have implications for understanding the mental chronometry of shared attention and social referencing.     

Differential modulation of neural activity throughout the distributed neural system for face perception in patients with Social Phobia and healthy subjects

Social Phobia (SP) is a marked and persistent fear of social or performance situations in which the person is exposed to unfamiliar people or to possible scrutiny by others. Faces of others are perceived as threatening by social phobic patients (SPP). To investigate how face processing is altered in the distributed neural system for face perception in Social Phobia, we designed an event-related fMRI study in which Healthy Controls (HC) and SPP were presented with angry, fearful, disgusted, happy and neutral faces and scrambled pictures (visual baseline). As compared to HC, SPP showed increased neural activity not only in regions involved in emotional processing including left amygdala and insula, as expected from previous reports, but also in the bilateral superior temporal sulcus (STS), a part of the core system for face perception that is involved in the evaluation of expression and personal traits. In addition SPP showed a significantly weaker activation in the left fusiform gyrus, left dorsolateral prefrontal cortex, and bilateral intraparietal sulcus as compared to HC. These effects were found not only in response to emotional faces but also to neutral faces as compared to scrambled pictures. Thus, SPP showed enhanced activity in brain areas related to processing of information about emotional expression and personality traits. In contrast, brain activity was decreased in areas for attention and for processing other information from the face, perhaps as a result of a feeling of wariness. These results indicate a differential modulation of neural activity throughout the different parts of the distributed neural system for face perception in SPP as compared to HC.     

Neural responses to emotional faces in women recovered from anorexia nervosa

Impairments in emotional processing have been associated with anorexia nervosa. However, it is unknown whether neural and behavioural differences in the processing of emotional stimuli persist following recovery. The aim of this study was to investigate the neural processing of emotional faces in individuals recovered from anorexia nervosa compared with healthy controls. Thirty-two participants (16 recovered anorexia nervosa, 16 healthy controls) underwent a functional magnetic resonance imaging (fMRI) scan. Participants viewed fearful and happy emotional faces and indicated the gender of the face presented. Whole brain analysis revealed no significant differences between the groups to the contrasts of fear versus happy and vice versa. Region of interest analysis demonstrated no significant differences in the neural response to happy or fearful stimuli between the groups in the amygdala or fusiform gyrus. These results suggest that processing of emotional faces may not be aberrant after recovery from anorexia nervosa.     

Preferential responses to faces in superior temporal and medial prefrontal cortex in three-year-old children

Perceiving faces and understanding emotions are key components of human social cognition. Prior research with adults and infants suggests that these social cognitive functions are supported by superior temporal cortex (STC) and medial prefrontal cortex (MPFC). We used functional near-infrared spectroscopy (fNIRS) to characterize functional responses in these cortical regions to faces in early childhood. Three-year-old children (n = 88, M(SD) = 3.15(.16) years) passively viewed faces that varied in emotional content and valence (happy, angry, fearful, neutral) and, for fearful and angry faces, intensity (100%, 40%), while undergoing fNIRS. Bilateral STC and MPFC showed greater oxygenated hemoglobin concentration values to all faces relative to objects. MPFC additionally responded preferentially to happy faces relative to neutral faces. We did not detect preferential responses to angry or fearful faces, or overall differences in response magnitude by emotional valence (100% happy vs. fearful and angry) or intensity (100% vs. 40% fearful and angry). In exploratory analyses, preferential responses to faces in MPFC were not robustly correlated with performance on tasks of early social cognition. These results link and extend adult and infant research on functional responses to faces in STC and MPFC and contribute to the characterization of the neural correlates of early social cognition.     

Exploring the nature of facial affect processing deficits in schizophrenia

Schizophrenia has been associated with deficits in facial affect processing, especially negative emotions. However, the exact nature of the deficit remains unclear. The aim of the present study was to investigate whether schizophrenia patients have problems in automatic allocation of attention as well as in controlled evaluation of facial affect. Thirty-seven patients with schizophrenia were compared with 41 control subjects on incidental facial affect processing (gender decision of faces with a fearful, angry, happy, disgusted, and neutral expression) and degraded facial affect labeling (labeling of fearful, angry, happy, and neutral faces). The groups were matched on estimates of verbal and performance intelligence (National Adult Reading Test; Raven's Matrices), general face recognition ability (Benton Face Recognition), and other demographic variables. The results showed that patients with schizophrenia as well as control subjects demonstrate the normal threat-related interference during incidental facial affect processing. Conversely, on controlled evaluation patients were specifically worse in the labeling of fearful faces. In particular, patients with high levels of negative symptoms may be characterized by deficits in labeling fear. We suggest that patients with schizophrenia show no evidence of deficits in the automatic allocation of attention resources to fearful (threat-indicating) faces, but have a deficit in the controlled processing of facial emotions that may be specific for fearful faces.     

Foveal and parafoveal spatial attention and its impact on the processing of facial expression: an ERP study

ObjectiveThe aim was to investigate the effects of spatial attention, stimulus location, and emotional expression on the processing of face stimuli.MethodsHealthy volunteers performed two sustained attention tasks, focusing their attention on either fixation (foveal location) or on a location several degrees above fixation (parafoveal location). Photographs of faces with either a neutral or a fearful expression were presented randomly at one of these locations. Event-related potentials were recorded in response to the face stimuli.ResultsSpatial attention modulated the early P1 and N1 components for both foveally and parafoveally presented stimuli. Emotional expression effects already occurred at the P1 stage in response to attended foveal stimuli, but only arose from 220 ms post-stimulus onwards in response to attended parafoveal stimuli. When faces were unattended, emotional expression effects were still present for parafoveal stimuli, whereas they were completely absent for foveal stimuli.ConclusionsThe modulations of the P1/N1 components by fearful faces are due to an early sensory modulation of extrastriate generators, and reflect an enhanced allocation of attention to threat-related stimuli.SignificanceFuture studies should take into account the possibility that spatial attention effects and effects of emotional expression processing are different for different positions in the visual field.     

Emergence of enhanced attention to fearful faces between 5 and 7 months of age

The adult brain is endowed with mechanisms subserving enhanced processing of salient emotional and social cues. Stimuli associated with threat represent one such class of cues. Previous research suggests that preferential allocation of attention to social signals of threat (i.e. a preference for fearful over happy facial expressions) emerges during the second half of the first year. The present study was designed to determine the age of onset for infants’ attentional bias for fearful faces. Allocation of attention was studied by measuring event-related potentials (ERPs) and looking times (in a visual paired comparison task) to fearful and happy faces in 5- and 7-month-old infants. In 7-month-olds, the preferential allocation of attention to fearful faces was evident in both ERPs and looking times, i.e. the negative central mid-latency ERP amplitudes were more negative, and the looking times were longer for fearful than happy faces. No such differences were observed in the 5-month-olds. It is suggested that an enhanced sensitivity to facial signals of threat emerges between 5 and 7 months of age, and it may reflect functional development of the neural mechanisms involved in processing of emotionally significant stimuli.     

Rapid influence of emotional scenes on encoding of facial expressions: an ERP study

In daily life, we perceive a person''s facial reaction as part of the natural environment surrounding it. Because most studies have investigated how facial expressions are recognized by using isolated faces, it is unclear what role the context plays. Although it has been observed that the N170 for facial expressions is modulated by the emotional context, it was not clear whether individuals use context information on this stage of processing to discriminate between facial expressions. The aim of the present study was to investigate how the early stages of face processing are affected by emotional scenes when explicit categorizations of fearful and happy facial expressions are made. Emotion effects were found for the N170, with larger amplitudes for faces in fearful scenes as compared to faces in happy and neutral scenes. Critically, N170 amplitudes were significantly increased for fearful faces in fearful scenes as compared to fearful faces in happy scenes and expressed in left-occipito-temporal scalp topography differences. Our results show that the information provided by the facial expression is combined with the scene context during the early stages of face processing.     

Emotional facial expressions reduce neural adaptation to face identity

In human social interactions, facial emotional expressions are a crucial source of information. Repeatedly presented information typically leads to an adaptation of neural responses. However, processing seems sustained with emotional facial expressions. Therefore, we tested whether sustained processing of emotional expressions, especially threat-related expressions, would attenuate neural adaptation. Neutral and emotional expressions (happy, mixed and fearful) of same and different identity were presented at 3 Hz. We used electroencephalography to record the evoked steady-state visual potentials (ssVEP) and tested to what extent the ssVEP amplitude adapts to the same when compared with different face identities. We found adaptation to the identity of a neutral face. However, for emotional faces, adaptation was reduced, decreasing linearly with negative valence, with the least adaptation to fearful expressions. This short and straightforward method may prove to be a valuable new tool in the study of emotional processing.     

Emotional object and scene stimuli modulate subsequent face processing: an event-related potential study

To understand the processing of facial expressions in terms of social communication, it is important to clarify how they are influenced by environmental stimuli such as natural scenes or objects. We investigated how and when neural responses to facial expressions were modulated by both a natural scene and an object containing emotional information. A facial expression stimulus (fearful/neutral) was presented after a scene or object stimulus (fearful/neutral), and then event-related potentials were recorded from both the onset of scene and facial expression presentation. As in previous studies, for the presentation of the scenes and objects positive-going waves at around 200-500 ms were observed for unpleasant visual stimuli at the Pz and Cz electrodes when the stimuli were intact; however, such a response was not observed when the stimuli were scrambled. During the subsequent facial expression presentation period, although we could not identify a significant interaction between the contextual information and facial expression in the N170 component, we observed a significant interaction in the P2 component: the P2 amplitude of the fearful cued was significantly larger than that of the neutral cued condition when the face was fearful, and the P2 amplitude of the neutral face was significantly larger than that of the fearful face condition when the preceding stimulus was neutral. These findings show that an adjacent, non-face stimulus containing emotional information influences the subsequent processing of facial expressions up to 260 ms, and even in cases when the two stimulus categories are different.     

Sustained happiness? Lack of repetition suppression in right-ventral visual cortex for happy faces

Emotional stimuli have been shown to preferentially engage initial attention but their sustained effects on neural processing remain largely unknown. The present study evaluated whether emotional faces engage sustained neural processing by examining the attenuation of neural repetition suppression to repeated emotional faces. Repetition suppression of neural function refers to the general reduction of neural activity when processing a repeated stimulus. Preferential processing of emotional face stimuli, however, should elicit sustained neural processing such that repetition suppression to repeated emotional faces is attenuated relative to faces with no emotional content. We measured the reduction of functional magnetic resonance imaging signals associated with immediate repetition of neutral, angry and happy faces. Whereas neutral faces elicited the greatest suppression in ventral visual cortex, followed by angry faces, repetition suppression was the most attenuated for happy faces. Indeed, happy faces showed almost no repetition suppression in part of the right-inferior occipital and fusiform gyri, which play an important role in face-identity processing. Our findings suggest that happy faces are associated with sustained visual encoding of face identity and thereby assist in the formation of more elaborate representations of the faces, congruent with findings in the behavioral literature.     

Elevated striatal and decreased dorsolateral prefrontal cortical activity in response to emotional stimuli in euthymic bipolar disorder: no associations with psychotropic medication load

Objective: To examine abnormal patterns of frontal cortical‐subcortical activity in response to emotional stimuli in euthymic individuals with bipolar disorder type I in order to identify trait‐like, pathophysiologic mechanisms of the disorder. We examined potential confounding effects of total psychotropic medication load and illness variables upon neural abnormalities. Method: We analyzed neural activity in 19 euthymic bipolar and 24 healthy individuals to mild and intense happy, fearful and neutral faces. Results: Relative to healthy individuals, bipolar subjects had significantly increased left striatal activity in response to mild happy faces (p < 0.05, corrected), decreased right dorsolateral prefrontal cortical (DLPFC) activity in response to neutral, mild and intense happy faces, and decreased left DLPFC activity in response to neutral, mild and intense fearful faces (p < 0.05, corrected). Bipolar and healthy individuals did not differ in amygdala activity in response to either emotion. In bipolar individuals, there was no significant association between medication load and abnormal activity in these regions, but a negative relationship between age of illness onset and amygdala activity in response to mild fearful faces (p = 0.007). Relative to those without comorbidities, bipolar individuals with comorbidities showed a trend increase in left striatal activity in response to mild happy faces. Conclusions: Abnormally increased striatal activity in response to potentially rewarding stimuli and decreased DLPFC activity in response to other emotionally salient stimuli may underlie mood instabilities in euthymic bipolar individuals, and are more apparent in those with comorbid diagnoses. No relationship between medication load and abnormal neural activity in bipolar individuals suggests that our findings may reflect pathophysiologic mechanisms of the illness rather than medication confounds. Future studies should examine whether this pattern of abnormal neural activity could distinguish bipolar from unipolar depression.