Gamma activation in young people with autism spectrum disorders and typically-developing controls when viewing emotions on faces

Background

Behavioural studies have highlighted irregularities in recognition of facial affect in children and young people with autism spectrum disorders (ASDs). Recent findings from studies utilising electroencephalography (EEG) and magnetoencephalography (MEG) have identified abnormal activation and irregular maintenance of gamma (>30 Hz) range oscillations when ASD individuals attempt basic visual and auditory tasks.

Methodology/Principal Fndings

The pilot study reported here is the first study to use spatial filtering techniques in MEG to explore face processing in children with ASD. We set out to examine theoretical suggestions that gamma activation underlying face processing may be different in a group of children and young people with ASD (n = 13) compared to typically developing (TD) age, gender and IQ matched controls. Beamforming and virtual electrode techniques were used to assess spatially localised induced and evoked activity. While lower-band (3–30 Hz) responses to faces were similar between groups, the ASD gamma response in occipital areas was observed to be largely absent when viewing emotions on faces. Virtual electrode analysis indicated the presence of intact evoked responses but abnormal induced activity in ASD participants.

Conclusions/Significance

These findings lend weight to previous suggestions that specific components of the early visual response to emotional faces is abnormal in ASD. Elucidation of the nature and specificity of these findings is worthy of further research.     

Culture Shapes Efficiency of Facial Age Judgments

Background

Cultural differences in socialization can lead to characteristic differences in how we perceive the world. Consistent with this influence of differential experience, our perception of faces (e.g., preference, recognition ability) is shaped by our previous experience with different groups of individuals.

Methodology/Principal Findings

Here, we examined whether cultural differences in social practices influence our perception of faces. Japanese, Chinese, and Asian-Canadian young adults made relative age judgments (i.e., which of these two faces is older?) for East Asian faces. Cross-cultural differences in the emphasis on respect for older individuals was reflected in participants'' latency in facial age judgments for middle-age adult faces—with the Japanese young adults performing the fastest, followed by the Chinese, then the Asian-Canadians. In addition, consistent with the differential behavioural and linguistic markers used in the Japanese culture when interacting with individuals younger than oneself, only the Japanese young adults showed an advantage in judging the relative age of children''s faces.

Conclusions/Significance

Our results show that different sociocultural practices shape our efficiency in processing facial age information. The impact of culture may potentially calibrate other aspects of face processing.     

Culture shapes how we look at faces

Background

Face processing, amongst many basic visual skills, is thought to be invariant across all humans. From as early as 1965, studies of eye movements have consistently revealed a systematic triangular sequence of fixations over the eyes and the mouth, suggesting that faces elicit a universal, biologically-determined information extraction pattern.

Methodology/Principal Findings

Here we monitored the eye movements of Western Caucasian and East Asian observers while they learned, recognized, and categorized by race Western Caucasian and East Asian faces. Western Caucasian observers reproduced a scattered triangular pattern of fixations for faces of both races and across tasks. Contrary to intuition, East Asian observers focused more on the central region of the face.

Conclusions/Significance

These results demonstrate that face processing can no longer be considered as arising from a universal series of perceptual events. The strategy employed to extract visual information from faces differs across cultures.     

Prolonged visual experience in adulthood modulates holistic face perception

Background

Using the well-known composite illusion as a marker of the holistic perception of faces, we tested how prolonged visual experience with a specific population of faces (4- to 6-year-old children) modulates the face perception system in adulthood.

Methodology/Principal Findings

We report a face composite effect that is larger for adult than children faces in a group of adults without experience with children faces (“children-face novices”), while it is of equal magnitude for adults and children faces in a population of preschool teachers (“children-face experts”). When considering preschool teachers only, we observed a significant correlation between the number of years of experience with children faces and the differential face composite effect between children and adults faces. Participants with at least 10 years of qualitative experience with children faces had a larger composite face effect for children than adult faces.

Conclusions/Significance

Overall, these observations indicate that even in adulthood face processes can be reshaped qualitatively, presumably to facilitate efficient processing of the differential morphological features of the frequently encountered population of faces.     

The Composite Task Reveals Stronger Holistic Processing in Children than Adults for Child Faces

Background

While own-age faces have been reported to be better recognized than other-age faces, the underlying cause of this phenomenon remains unclear. One potential cause is holistic face processing, a special kind of perceptual and cognitive processing reserved for perceiving upright faces. Previous studies have indeed found that adults show stronger holistic processing when looking at adult faces compared to child faces, but whether a similar own-age bias exists in children remains to be shown.

Methodology/Principal Findings

Here we used the composite face task – a standard test of holistic face processing – to investigate if, for child faces, holistic processing is stronger for children than adults. Results showed child participants (8–13 years) had a larger composite effect than adult participants (22–65 years).

Conclusions/Significance

Our finding suggests that differences in strength of holistic processing may underlie the own-age bias on recognition memory. We discuss the origin of own-age biases in terms of relative experience, face-space tuning, and social categorization.     

Face Coding Is Bilateral in the Female Brain

Background

It is currently believed that face processing predominantly activates the right hemisphere in humans, but available literature is very inconsistent.

Methodology/Principal Findings

In this study, ERPs were recorded in 50 right-handed women and men in response to 390 faces (of different age and sex), and 130 technological objects. Results showed no sex difference in the amplitude of N170 to objects; a much larger face-specific response over the right hemisphere in men, and a bilateral response in women; a lack of face-age coding effect over the left hemisphere in men, with no differences in N170 to faces as a function of age; a significant bilateral face-age coding effect in women.

Conclusions/Significance

LORETA reconstruction showed a significant left and right asymmetry in the activation of the fusiform gyrus (BA19), in women and men, respectively. The present data reveal a lesser degree of lateralization of brain functions related to face coding in women than men. In this light, they may provide an explanation of the inconsistencies in the available literature concerning the asymmetric activity of left and right occipito-temporal cortices devoted to face perception during processing of face identity, structure, familiarity or affective content.     

Age and the neural network of personal familiarity

Background

Accessing information that defines personally familiar context in real-world situations is essential for the social interactions and the independent functioning of an individual. Personal familiarity is associated with the availability of semantic and episodic information as well as the emotional meaningfulness surrounding a stimulus. These features are known to be associated with neural activity in distinct brain regions across different stimulus conditions (e.g., when perceiving faces, voices, places, objects), which may reflect a shared neural basis. Although perceiving context-rich personal familiarity may appear unchanged in aging on the behavioral level, it has not yet been studied whether this can be supported by neuroimaging data.

Methodology/Principal Findings

We used functional magnetic resonance imaging to investigate the neural network associated with personal familiarity during the perception of personally familiar faces and places. Twelve young and twelve elderly cognitively healthy subjects participated in the study. Both age groups showed a similar activation pattern underlying personal familiarity, predominantly in anterior cingulate and posterior cingulate cortices, irrespective of the stimulus type. The young subjects, but not the elderly subjects demonstrated an additional anterior cingulate deactivation when perceiving unfamiliar stimuli.

Conclusions/Significance

Although we found evidence for an age-dependent reduction in frontal cortical deactivation, our data show that there is a stimulus-independent neural network associated with personal familiarity of faces and places, which is less susceptible to aging-related changes.     

Influence of Repressive Coping Style on Cortical Activation during Encoding of Angry Faces

Background

Coping plays an important role for emotion regulation in threatening situations. The model of coping modes designates repression and sensitization as two independent coping styles. Repression consists of strategies that shield the individual from arousal. Sensitization indicates increased analysis of the environment in order to reduce uncertainty. According to the discontinuity hypothesis, repressors are sensitive to threat in the early stages of information processing. While repressors do not exhibit memory disturbances early on, they manifest weak memory for these stimuli later. This study investigates the discontinuity hypothesis using functional magnetic resonance imaging (fMRI).

Methods

Healthy volunteers (20 repressors and 20 sensitizers) were selected from a sample of 150 students on the basis of the Mainz Coping Inventory. During the fMRI experiment, subjects evaluated and memorized emotional and neutral faces. Subjects performed two sessions of face recognition: immediately after the fMRI session and three days later.

Results

Repressors exhibited greater activation of frontal, parietal and temporal areas during encoding of angry faces compared to sensitizers. There were no differences in recognition of facial emotions between groups neither immediately after exposure nor after three days.

Conclusions

The fMRI findings suggest that repressors manifest an enhanced neural processing of directly threatening facial expression which confirms the assumption of hyper-responsivity to threatening information in repression in an early processing stage. A discrepancy was observed between high neural activation in encoding-relevant brain areas in response to angry faces in repressors and no advantage in subsequent memory for these faces compared to sensitizers.     

Beauty hinders attention switch in change detection: the role of facial attractiveness and distinctiveness

Background

Recent research has shown that the presence of a task-irrelevant attractive face can induce a transient diversion of attention from a perceptual task that requires covert deployment of attention to one of the two locations. However, it is not known whether this spontaneous appraisal for facial beauty also modulates attention in change detection among multiple locations, where a slower, and more controlled search process is simultaneously affected by the magnitude of a change and the facial distinctiveness. Using the flicker paradigm, this study examines how spontaneous appraisal for facial beauty affects the detection of identity change among multiple faces.

Methodology/Principal Findings

Participants viewed a display consisting of two alternating frames of four faces separated by a blank frame. In half of the trials, one of the faces (target face) changed to a different person. The task of the participant was to indicate whether a change of face identity had occurred. The results showed that (1) observers were less efficient at detecting identity change among multiple attractive faces relative to unattractive faces when the target and distractor faces were not highly distinctive from one another; and (2) it is difficult to detect a change if the new face is similar to the old.

Conclusions/Significance

The findings suggest that attractive faces may interfere with the attention-switch process in change detection. The results also show that attention in change detection was strongly modulated by physical similarity between the alternating faces. Although facial beauty is a powerful stimulus that has well-demonstrated priority, its influence on change detection is easily superseded by low-level image similarity. The visual system appears to take a different approach to facial beauty when a task requires resource-demanding feature comparisons.     

Dealing with Feelings: Characterization of Trait Alexithymia on Emotion Regulation Strategies and Cognitive-Emotional Processing

Background

Alexithymia, or “no words for feelings”, is a personality trait which is associated with difficulties in emotion recognition and regulation. It is unknown whether this deficit is due primarily to regulation, perception, or mentalizing of emotions. In order to shed light on the core deficit, we tested our subjects on a wide range of emotional tasks. We expected the high alexithymics to underperform on all tasks.

Method

Two groups of healthy individuals, high and low scoring on the cognitive component of the Bermond-Vorst Alexithymia Questionnaire, completed questionnaires of emotion regulation and performed several emotion processing tasks including a micro expression recognition task, recognition of emotional prosody and semantics in spoken sentences, an emotional and identity learning task and a conflicting beliefs and emotions task (emotional mentalizing).

Results

The two groups differed on the Emotion Regulation Questionnaire, Berkeley Expressivity Questionnaire and Empathy Quotient. Specifically, the Emotion Regulation Quotient showed that alexithymic individuals used more suppressive and less reappraisal strategies. On the behavioral tasks, as expected, alexithymics performed worse on recognition of micro expressions and emotional mentalizing. Surprisingly, groups did not differ on tasks of emotional semantics and prosody and associative emotional-learning.

Conclusion

Individuals scoring high on the cognitive component of alexithymia are more prone to suppressive emotion regulation strategies rather than reappraisal strategies. Regarding emotional information processing, alexithymia is associated with reduced performance on measures of early processing as well as higher order mentalizing. However, difficulties in the processing of emotional language were not a core deficit in our alexithymic group.     

Neural correlates of enhanced visual short-term memory for angry faces: an FMRI study

Background

Fluid and effective social communication requires that both face identity and emotional expression information are encoded and maintained in visual short-term memory (VSTM) to enable a coherent, ongoing picture of the world and its players. This appears to be of particular evolutionary importance when confronted with potentially threatening displays of emotion - previous research has shown better VSTM for angry versus happy or neutral face identities.

Methodology/Principal Findings

Using functional magnetic resonance imaging, here we investigated the neural correlates of this angry face benefit in VSTM. Participants were shown between one and four to-be-remembered angry, happy, or neutral faces, and after a short retention delay they stated whether a single probe face had been present or not in the previous display. All faces in any one display expressed the same emotion, and the task required memory for face identity. We find enhanced VSTM for angry face identities and describe the right hemisphere brain network underpinning this effect, which involves the globus pallidus, superior temporal sulcus, and frontal lobe. Increased activity in the globus pallidus was significantly correlated with the angry benefit in VSTM. Areas modulated by emotion were distinct from those modulated by memory load.

Conclusions/Significance

Our results provide evidence for a key role of the basal ganglia as an interface between emotion and cognition, supported by a frontal, temporal, and occipital network.     

Emotional facial expression detection in the peripheral visual field

Background

In everyday life, signals of danger, such as aversive facial expressions, usually appear in the peripheral visual field. Although facial expression processing in central vision has been extensively studied, this processing in peripheral vision has been poorly studied.

Methodology/Principal Findings

Using behavioral measures, we explored the human ability to detect fear and disgust vs. neutral expressions and compared it to the ability to discriminate between genders at eccentricities up to 40°. Responses were faster for the detection of emotion compared to gender. Emotion was detected from fearful faces up to 40° of eccentricity.

Conclusions

Our results demonstrate the human ability to detect facial expressions presented in the far periphery up to 40° of eccentricity. The increasing advantage of emotion compared to gender processing with increasing eccentricity might reflect a major implication of the magnocellular visual pathway in facial expression processing. This advantage may suggest that emotion detection, relative to gender identification, is less impacted by visual acuity and within-face crowding in the periphery. These results are consistent with specific and automatic processing of danger-related information, which may drive attention to those messages and allow for a fast behavioral reaction.     

Attentional Prioritization of Infant Faces Is Limited to Own-Race Infants

Background

Recent evidence indicates that infant faces capture attention automatically, presumably to elicit caregiving behavior from adults and leading to greater probability of progeny survival. Elsewhere, evidence demonstrates that people show deficiencies in the processing of other-race relative to own-race faces. We ask whether this other-race effect impacts on attentional attraction to infant faces. Using a dot-probe task to reveal the spatial allocation of attention, we investigate whether other-race infants capture attention.

Principal Findings

South Asian and White participants (young adults aged 18–23 years) responded to a probe shape appearing in a location previously occupied by either an infant face or an adult face; across trials, the race (South Asian/White) of the faces was manipulated. Results indicated that participants were faster to respond to probes that appeared in the same location as infant faces than adult faces, but only on own-race trials.

Conclusions/Significance

Own-race infant faces attract attention, but other-race infant faces do not. Sensitivity to face-specific care-seeking cues in other-race kindenschema may be constrained by interracial contact and experience.     

The evolution of social orienting: evidence from chicks (Gallus gallus) and human newborns

Background

Converging evidence from different species indicates that some newborn vertebrates, including humans, have visual predispositions to attend to the head region of animate creatures. It has been claimed that newborn preferences for faces are domain-relevant and similar in different species. One of the most common criticisms of the work supporting domain-relevant face biases in human newborns is that in most studies they already have several hours of visual experience when tested. This issue can be addressed by testing newly hatched face-naïve chicks (Gallus gallus) whose preferences can be assessed prior to any other visual experience with faces.

Methods

In the present study, for the first time, we test the prediction that both newly hatched chicks and human newborns will demonstrate similar preferences for face stimuli over spatial frequency matched structured noise. Chicks and babies were tested using identical stimuli for the two species. Chicks underwent a spontaneous preference task, in which they have to approach one of two stimuli simultaneously presented at the ends of a runway. Human newborns participated in a preferential looking task.

Results and Significance

We observed a significant preference for orienting toward the face stimulus in both species. Further, human newborns spent more time looking at the face stimulus, and chicks preferentially approached and stood near the face-stimulus. These results confirm the view that widely diverging vertebrates possess similar domain-relevant biases toward faces shortly after hatching or birth and provide a behavioural basis for a comparison with neuroimaging studies using similar stimuli.     

Visual personal familiarity in amnestic mild cognitive impairment

Background

Patients with amnestic mild cognitive impairment are at high risk for developing Alzheimer''s disease. Besides episodic memory dysfunction they show deficits in accessing contextual knowledge that further specifies a general concept or helps to identify an object or a person.

Methodology/Principal Findings

Using functional magnetic resonance imaging, we investigated the neural networks associated with the perception of personal familiar faces and places in patients with amnestic mild cognitive impairment and healthy control subjects. Irrespective of stimulus type, patients compared to control subjects showed lower activity in right prefrontal brain regions when perceiving personally familiar versus unfamiliar faces and places. Both groups did not show different neural activity when perceiving faces or places irrespective of familiarity.

Conclusions/Significance

Our data highlight changes in a frontal cortical network associated with knowledge-based personal familiarity among patients with amnestic mild cognitive impairment. These changes could contribute to deficits in social cognition and may reduce the patients'' ability to transition from basic to complex situations and tasks.     

Dissociation of Neural Substrates of Response Inhibition to Negative Information between Implicit and Explicit Facial Go/Nogo Tasks: Evidence from an Electrophysiological Study

Background

Although ample evidence suggests that emotion and response inhibition are interrelated at the behavioral and neural levels, neural substrates of response inhibition to negative facial information remain unclear. Thus we used event-related potential (ERP) methods to explore the effects of explicit and implicit facial expression processing in response inhibition.

Methods

We used implicit (gender categorization) and explicit emotional Go/Nogo tasks (emotion categorization) in which neutral and sad faces were presented. Electrophysiological markers at the scalp and the voxel level were analyzed during the two tasks.

Results

We detected a task, emotion and trial type interaction effect in the Nogo-P3 stage. Larger Nogo-P3 amplitudes during sad conditions versus neutral conditions were detected with explicit tasks. However, the amplitude differences between the two conditions were not significant for implicit tasks. Source analyses on P3 component revealed that right inferior frontal junction (rIFJ) was involved during this stage. The current source density (CSD) of rIFJ was higher with sad conditions compared to neutral conditions for explicit tasks, rather than for implicit tasks.

Conclusions

The findings indicated that response inhibition was modulated by sad facial information at the action inhibition stage when facial expressions were processed explicitly rather than implicitly. The rIFJ may be a key brain region in emotion regulation.     

The other in me: interpersonal multisensory stimulation changes the mental representation of the self

Background

Recent studies have shown that the well-known effect of multisensory stimulation on body-awareness can be extended to self-recognition. Seeing someone else’s face being touched at the same time as one’s own face elicits changes in the mental representation of the self-face. We sought to further elucidate the underlying mechanisms and the effects of interpersonal multisensory stimulation (IMS) on the mental representation of the self and others.

Methodology/Principal Findings

Participants saw an unfamiliar face being touched synchronously or asynchronously with their own face, as if they were looking in the mirror. Following synchronous, but not asynchronous, IMS, participants assimilated features of the other’s face in the mental representation of their own face as evidenced by the change in the point of subjective equality for morphed pictures of the two faces. Interestingly, synchronous IMS resulted in a unidirectional change in the self-other distinction, affecting recognition of one’s own face, but not recognition of the other’s face. The participants’ autonomic responses to objects approaching the other’s face were higher following synchronous than asynchronous IMS, but this increase was not specific to the pattern of IMS in interaction with the viewed object. Finally, synchronous, as compared to asynchronous, IMS resulted in significant differences in participants’ ratings of their experience, but unlike other bodily illusions, positive changes in subjective experience were related to the perceived physical similarity between the two faces, and not to identification.

Conclusions/Significance

Synchronous IMS produces quantifiable changes in the mental representations of one’s face, as measured behaviorally. Changes in autonomic responses and in the subjective experience of self-identification were broadly consistent with patterns observed in other bodily illusions, but less robust. Overall, shared multisensory experiences between self and other can change the mental representation of one’s identity, and the perceived similarity of others relative to one’s self.     

Neural correlates of face and object perception in an awake chimpanzee (Pan troglodytes) examined by scalp-surface event-related potentials

Background

The neural system of our closest living relative, the chimpanzee, is a topic of increasing research interest. However, electrophysiological examinations of neural activity during visual processing in awake chimpanzees are currently lacking.

Methodology/Principal Findings

In the present report, skin-surface event-related brain potentials (ERPs) were measured while a fully awake chimpanzee observed photographs of faces and objects in two experiments. In Experiment 1, human faces and stimuli composed of scrambled face images were displayed. In Experiment 2, three types of pictures (faces, flowers, and cars) were presented. The waveforms evoked by face stimuli were distinguished from other stimulus types, as reflected by an enhanced early positivity appearing before 200 ms post stimulus, and an enhanced late negativity after 200 ms, around posterior and occipito-temporal sites. Face-sensitive activity was clearly observed in both experiments. However, in contrast to the robustly observed face-evoked N170 component in humans, we found that faces did not elicit a peak in the latency range of 150–200 ms in either experiment.

Conclusions/Significance

Although this pilot study examined a single subject and requires further examination, the observed scalp voltage patterns suggest that selective processing of faces in the chimpanzee brain can be detected by recording surface ERPs. In addition, this non-invasive method for examining an awake chimpanzee can be used to extend our knowledge of the characteristics of visual cognition in other primate species.