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The dynamic facial expressions of emotion automatically elicit multifaceted psychological activities; however, the temporal profiles and dynamic interaction patterns of brain activities remain unknown. We investigated these issues using magnetoencephalography. Participants passively observed dynamic facial expressions of fear and happiness, or dynamic mosaics. Source-reconstruction analyses utilizing functional magnetic-resonance imaging data revealed higher activation in broad regions of the bilateral occipital and temporal cortices in response to dynamic facial expressions than in response to dynamic mosaics at 150-200 ms and some later time points. The right inferior frontal gyrus exhibited higher activity for dynamic faces versus mosaics at 300-350 ms. Dynamic causal-modeling analyses revealed that dynamic faces activated the dual visual routes and visual-motor route. Superior influences of feedforward and feedback connections were identified before and after 200 ms, respectively. These results indicate that hierarchical, bidirectional neural network dynamics within a few hundred milliseconds implement the processing of dynamic facial expressions.

Emotional facial expressions are indispensable communicative tools, and social interactions involving facial expressions are impaired in some psychiatric disorders. Recent studies revealed that the perception of dynamic facial expressions was exaggerated in normal participants, and this exaggerated perception is weakened in autism spectrum disorder (ASD). Based on the notion that ASD and schizophrenia spectrum disorder are at two extremes of the continuum with respect to social impairment, we hypothesized that schizophrenic characteristics would strengthen the exaggerated perception of dynamic facial expressions. To test this hypothesis, we investigated the relationship between the perception of facial expressions and schizotypal traits in a normal population. We presented dynamic and static facial expressions, and asked participants to change an emotional face display to match the perceived final image. The presence of schizotypal traits was positively correlated with the degree of exaggeration for dynamic, as well as static, facial expressions. Among its subscales, the paranoia trait was positively correlated with the exaggerated perception of facial expressions. These results suggest that schizotypal traits, specifically the tendency to over-attribute mental states to others, exaggerate the perception of emotional facial expressions.

Previous electromyographic studies have reported that individuals with autism spectrum disorders (ASD) exhibited atypical patterns of facial muscle activity in response to facial expression stimuli. However, whether such activity is expressed in visible facial mimicry remains unknown. To investigate this issue, we videotaped facial responses in high-functioning individuals with ASD and controls to dynamic and static facial expressions of anger and happiness. Visual coding of facial muscle activity and the subjective impression ratings showed reduced congruent responses to dynamic expressions in the ASD group. Additionally, this decline was related to social dysfunction. These results suggest that impairment in overt facial mimicry in response to others' dynamic facial expressions may underlie difficulties in reciprocal social interaction among individuals with ASD.

This study investigated whether eye contact perception differs in people with different cultural backgrounds. Finnish (European) and Japanese (East Asian) participants were asked to determine whether Finnish and Japanese neutral faces with various gaze directions were looking at them. Further, participants rated the face stimuli for emotion and other affect-related dimensions. The results indicated that Finnish viewers had a smaller bias toward judging slightly averted gazes as directed at them when judging Finnish rather than Japanese faces, while the bias of Japanese viewers did not differ between faces from their own and other cultural backgrounds. This may be explained by Westerners experiencing more eye contact in their daily life leading to larger visual experience of gaze perception generally, and to more accurate perception of eye contact with people from their own cultural background particularly. The results also revealed cultural differences in the perception of emotion from neutral faces that could also contribute to the bias in eye contact perception.

Basal ganglia (BG) abnormalities are implicated in the pathophysiology of autism spectrum disorder (ASD). However, studies measuring the volume of the entire BG in individuals with ASD have reported discrepant findings, and no study conducted volume measurement of the entire substructures of the BG (the caudate, putamen, nucleus accumbens, and globus pallidus) in individuals with ASD. We delineated the BG substructures and measured their volumes in 29 adults with ASD without intellectual disabilities and 29 age- and gender-matched typically developed adult controls. We acquired T1-weighted anatomical images and performed semiautomated delineation and volume measurements of the above-mentioned subregions. Total cerebral volumes, sex, and ages were partialed out. Compared with controls, the putamen was significantly larger in the ASD group. The increased volume of the putamen found in high-functioning adults with ASD suggests that structural or histological abnormalities of the putamen may underlie the pathologies of ASD, such as repetitive and stereotyped behaviors and impaired social interactions.

Neuroimaging studies have found greater activation in the inferior occipital gyrus (IOG), or occipital face area, in response to faces relative to non-facial stimuli. However, the temporal, frequency, and functional profiles of IOG activity during face processing remain unclear. Here, this issue was investigated by recording intracranial field potentials in the IOG during the presentation of faces, mosaics, and houses in upright and inverted orientations. Time-frequency statistical parametric mapping analyses revealed greater gamma-band activation in the IOG beginning at 110 msec and covering 40-300 Hz in response to upright faces relative to upright houses and mosaics. Phase-amplitude cross-frequency coupling analyses revealed more evident theta-gamma couplings at 115-256 msec during the processing of upright faces as compared with that of upright houses and mosaics. Comparable gamma-band activity was observed during the processing of inverted and upright faces at about 100-200 msec, but weaker activity and different coupling with theta-band activity after 200 msec. These patterns of activity were more evident in the right than in the left IOG. These results, together with other evidence on neural communication, suggest that broadband gamma oscillations in the right IOG conduct rapid and multistage (i.e., both featural and configural) face processing in collaboration with theta oscillations transmitted from other brain regions., (Copyright © 2014 Elsevier Ltd. All rights reserved.)

Gaze and arrows automatically trigger attentional shifts. Neuroimaging studies have identified a commonality in the spatial distribution of the neural activation involved in such attentional shifts. However, it remains unknown whether these activations occur with common temporal profiles. To investigate this issue, magnetoencephalography (MEG) was used to evaluate neural activation involved in attentional shifts induced by gaze and arrows. MEG source reconstruction analyses revealed that the superior temporal sulcus and the inferior frontal gyrus were commonly activated after 200ms, in response to directional versus non-directional cues. Regression analyses further revealed that the magnitude of brain activity in these areas and in the bilateral occipital cortex was positively related to the effect of attentional shift on reaction times under both the gaze and the arrow conditions. The results also revealed that some brain regions were activated specifically in response to directional versus non-directional gaze or arrow cues at the 350-400ms time window. These results suggest that the neural mechanisms underlying attentional shifts induced by gaze and arrows share commonalities in their spatial distributions and temporal profiles, with some spatial differences at later time stages., (Copyright © 2014 Elsevier Ireland Ltd and the Japan Neuroscience Society. All rights reserved.)

This study aimed to evaluate the difference in non-predictive cues between gaze and arrows in attention orienting. Attention orienting was investigated with gaze or arrows as separate cues in a simple condition (i.e., block design) in Experiment 1 and in an unpredictable condition (i.e., randomized design) in Experiment 2. Two kinds of sound (voice and tone) stimuli were used as targets. Results showed that gaze and arrow cues induced enhanced attention orienting to a voice versus tone target in the block condition. However, in the randomized condition, enhanced attention orienting to a voice versus tone target was found in gaze but not arrow cues. The congruency of the meaning between a social cue (i.e., gaze) and a social target (i.e., voice) was clear in the randomized but not blocked design, because social gaze and non-social arrow cues were implemented in the same block. Thus, attention orienting might be mediated by the associated relationship of cue-target in a randomized condition, as an enhanced orienting effect was found when the associated relationship of cue-target was strong (i.e., social cue and target). The present study suggests that the difference in attention orienting between gaze and arrows is apparent in a randomized design (the unpredictable condition), and people employ a flexibly strategy of orienting to better respond to environmental changes., (Copyright © 2014 Elsevier B.V. All rights reserved.)

Behavioral studies have shown that emotional facial expressions are detected more rapidly and accurately than are neutral expressions. However, the neural mechanism underlying this efficient detection has remained unclear. To investigate this mechanism, we measured event-related potentials (ERPs) during a visual search task in which participants detected the normal emotional facial expressions of anger and happiness or their control stimuli, termed "anti-expressions," within crowds of neutral expressions. The anti-expressions, which were created using a morphing technique that produced changes equivalent to those in the normal emotional facial expressions compared with the neutral facial expressions, were most frequently recognized as emotionally neutral. Behaviorally, normal expressions were detected faster and more accurately and were rated as more emotionally arousing than were the anti-expressions. Regarding ERPs, the normal expressions elicited larger early posterior negativity (EPN) at 200-400ms compared with anti-expressions. Furthermore, larger EPN was related to faster and more accurate detection and higher emotional arousal. These data suggest that the efficient detection of emotional facial expressions is implemented via enhanced activation of the posterior visual cortices at 200-400ms based on their emotional significance., (Copyright © 2014 Elsevier B.V. All rights reserved.)

Background: Previous studies have shown that females and males differ in the processing of emotional facial expressions including the recognition of emotion, and that emotional facial expressions are detected more rapidly than are neutral expressions. However, whether the sexes differ in the rapid detection of emotional facial expressions remains unclear., Methodology/principal Findings: We measured reaction times (RTs) during a visual search task in which 44 females and 46 males detected normal facial expressions of anger and happiness or their anti-expressions within crowds of neutral expressions. Anti-expressions expressed neutral emotions with visual changes quantitatively comparable to normal expressions. We also obtained subjective emotional ratings in response to the facial expression stimuli. RT results showed that both females and males detected normal expressions more rapidly than anti-expressions and normal-angry expressions more rapidly than normal-happy expressions. However, females and males showed different patterns in their subjective ratings in response to the facial expressions. Furthermore, sex differences were found in the relationships between subjective ratings and RTs. High arousal was more strongly associated with rapid detection of facial expressions in females, whereas negatively valenced feelings were more clearly associated with the rapid detection of facial expressions in males., Conclusion: Our data suggest that females and males differ in their subjective emotional reactions to facial expressions and in the emotional processes that modulate the detection of facial expressions.

Human faces transmit multiple valuable signals, and neuroimaging studies have shown that the amygdala is active in response to facial stimuli. However, little has been known about the temporal profile of amygdala activation during facial signal processing until recently. Here we review three recent studies conducted by our group in which we recorded amygdala intracranial electroencephalography in humans. The subjects were engaged in tasks that required automatic processing of faces, eye gazes and emotional expressions. Time-frequency statistical parametric mapping analyses revealed that the amygdala showed gamma-band activation in response to emotional expressions, gazes and faces, with peak latencies at about 100 ms, 200 ms and 250 ms, respectively. These results suggest that: (1) the amygdala performs multiple-stage processing in response to these facial signals using different visual input routes, and (2) amygdala activation for processing all of these facial signals is rapid, which could be prior to or simultaneous with conscious awareness of faces.

Neuroimaging studies have reported greater activation of the human amygdala in response to faces than to nonfacial stimuli, yet little is known about the temporal profile of this activation. We investigated this issue by recording the intracranial field potentials of the amygdala in participants undergoing preneurosurgical assessment (n = 6). Participants observed faces, mosaics, and houses in upright and inverted orientations using a dummy target detection task. Time-frequency statistical parametric mapping analyses revealed that the amygdala showed greater gamma-band activity in response to faces than to mosaics at 200-300 msec, with a peak at 255 msec. Gamma-band activation with a similar temporal profile was also found in response to faces versus houses. Activation patterns did not differ between upright and inverted presentations of stimuli. These results suggest that the human amygdala is involved in the early stages of face processing, including the modulation of subjective perception of faces.

Neuroimaging studies have reported greater activation of the human amygdala in response to emotional facial expressions, especially for fear. However, little is known about how fast this activation occurs. We investigated this issue by recording the intracranial field potentials of the amygdala in subjects undergoing pre-neurosurgical assessment (n=6). The subjects observed fearful, happy, and neutral facial expressions. Time-frequency statistical parametric mapping analyses revealed that the amygdala showed greater gamma-band activity in response to fearful compared with neutral facial expressions at 50-150 ms, with a peak at 135 ms. These results indicate that the human amygdala is able to rapidly process fearful facial expressions., (Copyright © 2010 Elsevier Ltd. All rights reserved.)

Several studies have examined facial expression recognition in pervasive developmental disorder (PDD), including autism and Asperger's disorder, but the results have been inconsistent. We investigated the relationship between facial expression recognition and age, face recognition, and symptom severity. Subjects were 28 individuals with mild PDD subtypes and 28 age- and gender-matched controls. Among six emotions, fearful expression recognition was specifically impaired in PDD subjects. Age had positive effects on fearful expression recognition directly and indirectly via the development of face recognition in controls, but not in PDD subjects. Furthermore, fearful expression recognition was related to the severity of PDD symptoms. We conclude that individuals with PDD show an atypical development of facial expression recognition. Moreover, impaired fearful expression recognition is closely related to social dysfunction.

Current research increasingly suggests that spatial cognition in humans is accomplished by many specialized mechanisms, each designed to solve a particular adaptive problem. A major adaptive problem for our hominin ancestors, particularly females, was the need to efficiently gather immobile foods which could vary greatly in quality, quantity, spatial location and temporal availability. We propose a cognitive model of a navigational gathering adaptation in humans and test its predictions in samples from the US and Japan. Our results are uniformly supportive: the human mind appears equipped with a navigational gathering adaptation that encodes the location of gatherable foods into spatial memory. This mechanism appears to be chronically active in women and activated under explicit motivation in men.

Background: The eye gaze of other individuals conveys important social information and can trigger multiple psychological activities; some of which, such as emotional reactions and attention orienting, occur very rapidly. Although some neuroscientific evidence has suggested that the amygdala may be involved in such rapid gaze processing, no evidence has been reported concerning the speed at which the amygdala responds to eye gaze., Methodology/principal Findings: To investigate this issue, we recorded electrical activity within the amygdala of six subjects using intracranial electrodes. Subjects observed images of eyes and mosaics pointing in averted and straight directions. The amygdala showed higher gamma-band oscillations for eye gaze than for mosaics, which peaked at 200 ms regardless of the direction of the gaze., Conclusion: These results indicate that the human amygdala rapidly processes eye gaze.

Neuroimaging studies suggest that the amygdala integrates emotional expression and gaze direction, but the findings are inconsistent. We hypothesized that the dynamic facial expressions, which are more salient stimuli than static facial expressions are, would reveal the integration of emotional expression and gaze direction in amygdala activity. To test this hypothesis, we presented dynamic and static facial expressions of anger and happiness looking toward and away from the subject, and we visualized brain activity during these presentations using functional magnetic resonance imaging (fMRI). After the image acquisition phase of the study, the subject's experienced emotion in response to each stimulus was investigated. The left amygdala showed an interaction between presentation condition and gaze direction, indicating higher activity in response to dynamic, but not static, expressions looking toward the subjects than to expressions looking away from them. This was true for both angry and happy expressions. This pattern corresponded with the intensity of emotional arousal. These results suggest that the amygdala integrates emotional expression and gaze direction in dynamic facial expressions and modulates emotional arousal., (2010 Elsevier Inc. All rights reserved.)

Individuals with pervasive developmental disorder (PDD) have difficulty with social communication via emotional facial expressions, but behavioral studies involving static images have reported inconsistent findings about emotion recognition. We investigated whether dynamic presentation of facial expression would enhance subjective perception of expressed emotion in 13 individuals with PDD and 13 typically developing controls. We presented dynamic and static emotional (fearful and happy) expressions. Participants were asked to match a changeable emotional face display with the last presented image. The results showed that both groups perceived the last image of dynamic facial expression to be more emotionally exaggerated than the static facial expression. This finding suggests that individuals with PDD have an intact perceptual mechanism for processing dynamic information in another individual's face.

Background: Previous reports have suggested impairment in facial expression recognition in delinquents, but controversy remains with respect to how such recognition is impaired. To address this issue, we investigated facial expression recognition in delinquents in detail., Methods: We tested 24 male adolescent/young adult delinquents incarcerated in correctional facilities. We compared their performances with those of 24 age- and gender-matched control participants. Using standard photographs of facial expressions illustrating six basic emotions, participants matched each emotional facial expression with an appropriate verbal label., Results: Delinquents were less accurate in the recognition of facial expressions that conveyed disgust than were control participants. The delinquents misrecognized the facial expressions of disgust as anger more frequently than did controls., Conclusion: These results suggest that one of the underpinnings of delinquency might be impaired recognition of emotional facial expressions, with a specific bias toward interpreting disgusted expressions as hostile angry expressions.

Eye gaze, hand-pointing gestures, and arrows automatically trigger attentional shifts. Although it has been suggested that common neural mechanisms underlie these three types of attentional shifts, this issue remains unsettled. We measured brain activity using fMRI while participants observed directional and non-directional stimuli, including eyes, hands, and arrows, to investigate this issue. Conjunction analyses revealed that the posterior superior temporal sulcus (STS), the inferior parietal lobule, the inferior frontal gyrus, and the occipital cortices in the right hemisphere were more active in common in response to directional versus non-directional stimuli. These results suggest commonalities in the neurocognitive mechanisms underlying the automatic attentional shifts triggered by gaze, gestures, and symbols.

The human superior temporal sulcus (STS) has been suggested to be involved in gaze processing, but temporal data regarding this issue are lacking. We investigated this topic by combining fMRI and MEG in four normal subjects. Photographs of faces with either averted or straight eye gazes were presented and subjects passively viewed the stimuli. First, we analyzed the brain areas involved using fMRI. A group analysis revealed activation of the STS for averted compared to straight gazes, which was confirmed in all subjects. We then measured brain activity using MEG, and conducted a 3D spatial filter analysis. The STS showed higher activity in response to averted versus straight gazes during the 150-200 ms period, peaking at around 170 ms, after stimulus onset. In contrast, the fusiform gyrus, which was detected by the main effect of stimulus presentations in fMRI analysis, exhibited comparable activity across straight and averted gazes at about 170 ms. These results indicate involvement of the human STS in rapid processing of the eye gaze of another individual.