Effects of unconscious processing on implicit memory for fearful faces

Emotional stimuli can be processed even when participants perceive them without conscious awareness, but the extent to which unconsciously processed emotional stimuli influence implicit memory after short and long delays is not fully understood. We addressed this issue by measuring a subliminal affective priming effect in Experiment 1 and a long-term priming effect in Experiment 2. In Experiment 1, a flashed fearful or neutral face masked by a scrambled face was presented three times, then a target face (either fearful or neutral) was presented and participants were asked to make a fearful/neutral judgment. We found that, relative to a neutral prime face (neutral-fear face), a fearful prime face speeded up participants' reaction to a fearful target (fear-fear face), when they were not aware of the masked prime face. But this response pattern did not apply to the neutral target. In Experiment 2, participants were first presented with a masked faces six times during encoding. Three minutes later, they were asked to make a fearful/neutral judgment for the same face with congruent expression, the same face with incongruent expression or a new face. Participants showed a significant priming effect for the fearful faces but not for the neutral faces, regardless of their awareness of the masked faces during encoding. These results provided evidence that unconsciously processed stimuli could enhance emotional memory after both short and long delays. It indicates that emotion can enhance memory processing whether the stimuli are encoded consciously or unconsciously.     

Face perception: domain specific, not process specific

Evidence that face perception is mediated by special cognitive and neural mechanisms comes from fMRI studies of the fusiform face area (FFA) and behavioral studies of the face inversion effect. Here, we used these two methods to ask whether face perception mechanisms are stimulus specific, process specific, or both. Subjects discriminated pairs of upright or inverted faces or house stimuli that differed in either the spatial distance among parts (configuration) or the shape of the parts. The FFA showed a much higher response to faces than to houses, but no preference for the configuration task over the part task. Similarly, the behavioral inversion effect was as large in the part task as the configuration task for faces, but absent in both part and configuration tasks for houses. These findings indicate that face perception mechanisms are not process specific for parts or configuration but are domain specific for face stimuli per se.     

Frontal EEG Activation Asymmetry Reflects Cognitive Biases in Anxiety: Evidence from an Emotional Face Stroop Task

Electroencephalography (EEG) has been extensively used in studies of the frontal asymmetry of emotion and motivation. This study investigated the midfrontal EEG activation, heart rate and skin conductance during an emotional face analog of the Stroop task, in anxious and non-anxious participants. In this task, the participants were asked to identify the expression of calm, fearful and happy faces that had either a congruent or incongruent emotion name written across them. Anxious participants displayed a cognitive bias characterized by facilitated attentional engagement with fearful faces. Fearful face trials induced greater relative right frontal activation, whereas happy face trials induced greater relative left frontal activation. Moreover, anxiety specifically modulated the magnitude of the right frontal activation to fearful faces, which also correlated with the cognitive bias. Therefore, these results show that frontal EEG activation asymmetry reflects the bias toward facilitated processing of fearful faces in anxiety.     

面孔分类中空间高低频表征的神经机制：一个颅内脑电研究

来自多方面的研究表明,面孔的分类和识别位于特定脑区．同时,已有行为实验研究表明,图像的空间高低频特征在面孔分类的不同范畴中起不同的贡献,例如身份更多被低频信号传递,性别被高低频共同传递,而表情更多被高频传递．然而,空间频率在面孔分类中的贡献,其表征和神经机制目前相关研究很少．利用特定癫痫患者植入颅内电极的监控期,呈现不同类型面孔图像,同时记录其颅内脑电,用事件相关电位方法考察了据认为是面孔特定成分的相关电位的潜伏期在170 ms的波形(N170波形)的变化;用电极反应显著性分析考察了空间频率在不同分类特征上的贡献．结果表明,空间高频(HSF)图像的N170潜伏期显著延迟．只呈现空间低频(LSF)图像,N170的潜伏期对普通人面孔会延迟,而对熟悉的名人则没有这个差异．女性面孔诱发的N170在HSF条件下潜伏期明显晚于LSF条件,而男性面孔诱发的波形则不存在这个差异．表情在N170上没有体现出任何差异．但是基于电极的显著性分析表明,有更多的额叶电极参与了表情的加工;身份特征加工有更多电极在空间低频上表现出差异,而性别加工则空间高低频比较平衡．与以往行为结果不同的是,表情加工也有更多低频贡献,而且表情的差异可以在早达114 ms的时候就发生．这符合表情信息在颞枕区域有一个快速基本加工,再传递到其他脑区的认知模型．因此,空间高低频信息在身份和性别上的贡献,可能发生在经典的面孔加工脑区,由N170表达,表情信息不由N170表达,而是在颞枕较广泛的范围内快速加工再传递到别的脑区,如额叶．这是首次利用颅内脑电就空间频率在面孔分类中的贡献的神经机制进行研究,为深入理解脑内面孔各种特征加工的动态过程提供了一个新的切入点．     

Baboons (Papio papio) spontaneously process the first-order but not second-order configural properties of faces

A two-alternative forced-choice discrimination task was used to assess whether baboons (N=7) spontaneously process qualitative (i.e., first-order) or quantitative (i.e., second-order) variations in the configural arrangement of facial features. Experiment 1 used as test stimuli second-order pictorial faces of humans or baboons in which the mouth and the eyes were rotated upside down relative to the normal face. Baboons readily discriminated two different normal faces but did not discriminate a normal face from its second-order modified version. Experiment 2 used human or baboon faces for which the first-order configural properties had been distorted by reversing the location of the eyes and mouth within the face. Discrimination was prompt with these stimuli. Experiment 3 replicated some of the conditions and the results of experiment 1, thus ruling out possible effects of learning. It is concluded that baboons are more adept at spontaneously processing first- than second-order configural facial properties, similar to what is known in the human developmental literature.     

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.     

Modulation of Alpha Oscillations in the Human EEG with Facial Preference

Facial preference that results from the processing of facial information plays an important role in social interactions as well as the selection of a mate, friend, candidate, or favorite actor. However, it still remains elusive which brain regions are implicated in the neural mechanisms underlying facial preference, and how neural activities in these regions are modulated during the formation of facial preference. In the present study, we investigated the modulation of electroencephalography (EEG) oscillatory power with facial preference. For the reliable assessments of facial preference, we designed a series of passive viewing and active choice tasks. In the former task, twenty-four face stimuli were passively viewed by participants for multiple times in random order. In the latter task, the same stimuli were then evaluated by participants for their facial preference judgments. In both tasks, significant differences between the preferred and non-preferred faces groups were found in alpha band power (8–13 Hz) but not in other frequency bands. The preferred faces generated more decreases in alpha power. During the passive viewing task, significant differences in alpha power between the preferred and non-preferred face groups were observed at the left frontal regions in the early (0.15–0.4 s) period during the 1-s presentation. By contrast, during the active choice task when participants consecutively watched the first and second face for 1 s and then selected the preferred one, an alpha power difference was found for the late (0.65–0.8 s) period over the whole brain during the first face presentation and over the posterior regions during the second face presentation. These results demonstrate that the modulation of alpha activity by facial preference is a top-down process, which requires additional cognitive resources to facilitate information processing of the preferred faces that capture more visual attention than the non-preferred faces.     

The hatching larva of the priapulid worm Halicryptus spinulosus

Background

Faces, as socially relevant stimuli, readily capture human visuospatial attention. Although faces also play important roles in the social lives of chimpanzees, the closest living species to humans, the way in which faces are attentionally processed remains unclear from a comparative-cognitive perspective. In the present study, three young chimpanzees (Pan troglodytes) were tested with a simple manual response task in which various kinds of photographs, including faces as non-informative cues, were followed by a target.

Results

When the target appeared at the location that had been occupied by the face immediately before target onset, response times were significantly faster than when the target appeared at the opposite location that had been by the other object. Such an advantage was not observed when a photograph of a banana was paired with the other object. Furthermore, this attentional capture was also observed when upright human faces were presented, indicating that this effect is not limited to own-species faces. On the contrary, when the participants were tested with inverted chimpanzee faces, this effect was rather weakened, suggesting the specificity to upright faces.

Conclusion

Chimpanzee's visuospatial attention was easily captured by the face stimuli. This effect was face specific and stronger for upright faces than inverted. These results are consistent with those from typically developing humans.     

A new approach to the diagnosis of deficits in processing faces: Potential application in autism research

Deficits in social communication are one of the behavioral signatures of autism spectrum disorder(ASD). Because faces are arguably the most important social stimuli that we encounter in everyday life, investigating the ability of individuals with ASD to process faces is thought to be important for understanding the nature of ASD. However, although a considerable body of evidence suggests that ASD individuals show specific impairments in face processing, a significant number of studies argue otherwise. Through a literature review, we found that this controversy is largely attributable to the different face tests used across different studies. Therefore, a more reliable and valid face test is needed. To this end, we performed a meta-analysis on data gleaned from a variety of face tests conducted on individuals with developmental prosopagnosia(DP) who suffer a selective deficit in face processing. Based on this meta-analysis, we selected an old/new face recognition test that relies on face memory as a standard diagnostic test for measuring specific face processing deficits. This test not only reliably reflects DP individuals' subjective experiences with faces in their daily lives, but also effectively differentiates deficits in face processing from deficits caused by other general problems. In addition, DP individuals' performance in this test predicts their performance in a variety of face tests that examine specific components of face processing(e.g., holistic processing of faces). Finally, this test can be easily administrated and is not overly sensitive to prior knowledge. In summary, this test can be used to evaluate face-processing ability, and it helped to resolve the controversy whether individuals with ASD exhibit face-processing deficits.     

Reduced Face Aftereffects in Autism Are Not Due to Poor Attention

This study aimed to determine why face identity aftereffects are diminished in children with autism, relative to typical children. To address the possibility that reduced face aftereffects might reflect reduced attention to adapting stimuli, we investigated the consequence of controlling attention to adapting faces during a face identity aftereffect task in children with autism and typical children. We also included a size-change between adaptation and test stimuli to determine whether the reduced aftereffects reflect atypical adaptation to low- or higher-level stimulus properties. Results indicated that when attention was controlled and directed towards adapting stimuli, face identity aftereffects in children with autism were significantly reduced relative to typical children. This finding challenges the notion that atypicalities in the quality and/or quantity of children’s attention during adaptation might account for group differences previously observed in this paradigm. Additionally, evidence of diminished face identity aftereffects despite a stimulus size change supports an adaptive processing atypicality in autism that extends beyond low-level, retinotopically coded stimulus properties. These findings support the notion that diminished face aftereffects in autism reflect atypicalities in adaptive norm-based coding, which could also contribute to face processing difficulties in this group.     

Effects of attention and emotion on face processing in the human brain: an event-related fMRI study.

We used event-related fMRI to assess whether brain responses to fearful versus neutral faces are modulated by spatial attention. Subjects performed a demanding matching task for pairs of stimuli at prespecified locations, in the presence of task-irrelevant stimuli at other locations. Faces or houses unpredictably appeared at the relevant or irrelevant locations, while the faces had either fearful or neutral expressions. Activation of fusiform gyri by faces was strongly affected by attentional condition, but the left amygdala response to fearful faces was not. Right fusiform activity was greater for fearful than neutral faces, independently of the attention effect on this region. These results reveal differential influences on face processing from attention and emotion, with the amygdala response to threat-related expressions unaffected by a manipulation of attention that strongly modulates the fusiform response to faces.     

The Part Task of the Part-Spacing Paradigm Is Not a Pure Measurement of Part-Based Information of Faces

Background

Faces are arguably one of the most important object categories encountered by human observers, yet they present one of the most difficult challenges to both the human and artificial visual systems. A variety of experimental paradigms have been developed to study how faces are represented and recognized, among which is the part-spacing paradigm. This paradigm is presumed to characterize the processing of both the featural and configural information of faces, and it has become increasingly popular for testing hypotheses on face specificity and in the diagnosis of face perception in cognitive disorders.

Methodology/Principal Findings

In two experiments we questioned the validity of the part task of this paradigm by showing that, in this task, measuring pure information about face parts is confounded by the effect of face configuration on the perception of those parts. First, we eliminated or reduced contributions from face configuration by either rearranging face parts into a non-face configuration or by removing the low spatial frequencies of face images. We found that face parts were no longer sensitive to inversion, suggesting that the previously reported inversion effect observed in the part task was due in fact to the presence of face configuration. Second, self-reported prosopagnosic patients who were selectively impaired in the holistic processing of faces failed to detect part changes when face configurations were presented. When face configurations were scrambled, however, their performance was as good as that of normal controls.

Conclusions/Significance

In sum, consistent evidence from testing both normal and prosopagnosic subjects suggests the part task of the part-spacing paradigm is not an appropriate task for either measuring how face parts alone are processed or for providing a valid contrast to the spacing task. Therefore, conclusions from previous studies using the part-spacing paradigm may need re-evaluation with proper paradigms.     

Effect of Familiarity on Reward Anticipation in Children with and without Autism Spectrum Disorders

Background

Previous research on the reward system in autism spectrum disorders (ASD) suggests that children with ASD anticipate and process social rewards differently than typically developing (TD) children—but has focused on the reward value of unfamiliar face stimuli. Children with ASD process faces differently than their TD peers. Previous research has focused on face processing of unfamiliar faces, but less is known about how children with ASD process familiar faces. The current study investigated how children with ASD anticipate rewards accompanied by familiar versus unfamiliar faces.

Methods

The stimulus preceding negativity (SPN) of the event-related potential (ERP) was utilized to measure reward anticipation. Participants were 6- to 10-year-olds with (N = 14) and without (N = 14) ASD. Children were presented with rewards accompanied by incidental face or non-face stimuli that were either familiar (caregivers) or unfamiliar. All non-face stimuli were composed of scrambled face elements in the shape of arrows, controlling for visual properties.

Results

No significant differences between familiar versus unfamiliar faces were found for either group. When collapsing across familiarity, TD children showed larger reward anticipation to face versus non-face stimuli, whereas children with ASD did not show differential responses to these stimulus types. Magnitude of reward anticipation to faces was significantly correlated with behavioral measures of social impairment in the ASD group.

Conclusions

The findings do not provide evidence for differential reward anticipation for familiar versus unfamiliar face stimuli in children with or without ASD. These findings replicate previous work suggesting that TD children anticipate rewards accompanied by social stimuli more than rewards accompanied by non-social stimuli. The results do not support the idea that familiarity normalizes reward anticipation in children with ASD. Our findings also suggest that magnitude of reward anticipation to faces is correlated with levels of social impairment for children with ASD.     

Observed Touch on a Non-Human Face Is Not Remapped onto the Human Observer's Own Face

Visual remapping of touch (VRT) is a phenomenon in which seeing a human face being touched enhances detection of tactile stimuli on the observer''s own face, especially when the observed face expresses fear. This study tested whether VRT would occur when seeing touch on monkey faces and whether it would be similarly modulated by facial expressions. Human participants detected near-threshold tactile stimulation on their own cheeks while watching fearful, happy, and neutral human or monkey faces being concurrently touched or merely approached by fingers. We predicted minimal VRT for neutral and happy monkey faces but greater VRT for fearful monkey faces. The results with human faces replicated previous findings, demonstrating stronger VRT for fearful expressions than for happy or neutral expressions. However, there was no VRT (i.e. no difference between accuracy in touch and no-touch trials) for any of the monkey faces, regardless of facial expression, suggesting that touch on a non-human face is not remapped onto the somatosensory system of the human observer.     

Social status gates social attention in humans

Humans tend to shift attention in response to the averted gaze of a face they are fixating, a phenomenon known as gaze cuing. In the present paper, we aimed to address whether the social status of the cuing face modulates this phenomenon. Participants were asked to look at the faces of 16 individuals and read fictive curriculum vitae associated with each of them that could describe the person as having a high or low social status. The association between each specific face and either high or low social status was counterbalanced between participants. The same faces were then used as stimuli in a gaze-cuing task. The results showed a greater gaze-cuing effect for high-status faces than for low-status faces, independently of the specific identity of the face. These findings confirm previous evidence regarding the important role of social factors in shaping social attention and show that a modulation of gaze cuing can be observed even when knowledge about social status is acquired through episodic learning.     

Recognition of monkey faces by monkey experts

Human beings automatically discriminate human faces at the individual level. Infants aged 3 months implicitly recognise monkey faces, but this capacity disappears as recognition skills mature. Expertise is known to affect recognition capacities for different categories of stimuli that are not even face-like in their configuration. We have explored the capacity of adult experts and non-experts in primatology to recognise monkey faces in both explicit and implicit recognition tasks. In the explicit task, where subjects received the instruction to recognise a face seen previously, experts proved to be more accurate than non-experts. Experts were more affected by inversion than non-experts, suggesting that the processing of those faces is based on their configuration, as is generally observed for human faces. This replicates findings from Diamond and Carey (J Exp Psychol Gen 115:107–117, 1986) in dog experts. In the implicit recognition task, assessed by a visual paired comparison task where no instruction of recognition was given, automatic discrimination was observed for human faces but not for monkey faces. These results suggest that experience acquired by the time of adulthood did not lead the experts to develop recognition skills to the point of matching those exhibited for human faces.     

Sequential Effects in Judgements of Attractiveness: The Influences of Face Race and Sex

In perceptual decision-making, a person’s response on a given trial is influenced by their response on the immediately preceding trial. This sequential effect was initially demonstrated in psychophysical tasks, but has now been found in more complex, real-world judgements. The similarity of the current and previous stimuli determines the nature of the effect, with more similar items producing assimilation in judgements, while less similarity can cause a contrast effect. Previous research found assimilation in ratings of facial attractiveness, and here, we investigated whether this effect is influenced by the social categories of the faces presented. Over three experiments, participants rated the attractiveness of own- (White) and other-race (Chinese) faces of both sexes that appeared successively. Through blocking trials by race (Experiment 1), sex (Experiment 2), or both dimensions (Experiment 3), we could examine how sequential judgements were altered by the salience of different social categories in face sequences. For sequences that varied in sex alone, own-race faces showed significantly less opposite-sex assimilation (male and female faces perceived as dissimilar), while other-race faces showed equal assimilation for opposite- and same-sex sequences (male and female faces were not differentiated). For sequences that varied in race alone, categorisation by race resulted in no opposite-race assimilation for either sex of face (White and Chinese faces perceived as dissimilar). For sequences that varied in both race and sex, same-category assimilation was significantly greater than opposite-category. Our results suggest that the race of a face represents a superordinate category relative to sex. These findings demonstrate the importance of social categories when considering sequential judgements of faces, and also highlight a novel approach for investigating how multiple social dimensions interact during decision-making.     

How Well Do Computer-Generated Faces Tap Face Expertise?

The use of computer-generated (CG) stimuli in face processing research is proliferating due to the ease with which faces can be generated, standardised and manipulated. However there has been surprisingly little research into whether CG faces are processed in the same way as photographs of real faces. The present study assessed how well CG faces tap face identity expertise by investigating whether two indicators of face expertise are reduced for CG faces when compared to face photographs. These indicators were accuracy for identification of own-race faces and the other-race effect (ORE)–the well-established finding that own-race faces are recognised more accurately than other-race faces. In Experiment 1 Caucasian and Asian participants completed a recognition memory task for own- and other-race real and CG faces. Overall accuracy for own-race faces was dramatically reduced for CG compared to real faces and the ORE was significantly and substantially attenuated for CG faces. Experiment 2 investigated perceptual discrimination for own- and other-race real and CG faces with Caucasian and Asian participants. Here again, accuracy for own-race faces was significantly reduced for CG compared to real faces. However the ORE was not affected by format. Together these results signal that CG faces of the type tested here do not fully tap face expertise. Technological advancement may, in the future, produce CG faces that are equivalent to real photographs. Until then caution is advised when interpreting results obtained using CG faces.     

Emotional expectations influence neural sensitivity to fearful faces in humans: An event-related potential study

The present study tested whether neural sensitivity to salient emotional facial expressions was influenced by emotional expectations induced by a cue that validly predicted the expression of a subsequently presented target face. Event-related potentials (ERPs) elicited by fearful and neutral faces were recorded while participants performed a gender discrimination task under cued (‘expected’) and uncued (‘unexpected’) conditions. The behavioral results revealed that accuracy was lower for fearful compared with neutral faces in the unexpected condition, while accuracy was similar for fearful and neutral faces in the expected condition. ERP data revealed increased amplitudes in the P2 component and 200–250 ms interval for unexpected fearful versus neutral faces. By contrast, ERP responses were similar for fearful and neutral faces in the expected condition. These findings indicate that human neural sensitivity to fearful faces is modulated by emotional expectations. Although the neural system is sensitive to unpredictable emotionally salient stimuli, sensitivity to salient stimuli is reduced when these stimuli are predictable.     

Mental fatigue modulates dynamic adaptation to perceptual demand in speeded detection

When stimulus intensity in simple reaction-time tasks randomly varies across trials, detection speed usually improves after a low-intensity trial. With auditory stimuli, this improvement was often found to be asymmetric, being greater on current low-intensity trials. Our study investigated (1) whether asymmetric sequential intensity adaptation also occurs with visual stimuli; (2) whether these adjustments reflect decision-criterion shifts or, rather, a modulation of perceptual sensitivity; and (3) how sequential intensity adaptation and its underlying mechanisms are affected by mental fatigue induced through prolonged performance. In a continuous speeded detection task with randomly alternating high- and low-intensity visual stimuli, the reaction-time benefit after low-intensity trials was greater on subsequent low- than high-intensity trials. This asymmetry, however, only developed with time on task (TOT). Signal-detection analyses showed that the decision criterion transiently became more liberal after a low-intensity trial, whereas observer sensitivity increased when the preceding and current stimulus were of equal intensity. TOT-induced mental fatigue only affected sensitivity, which dropped more on low- than on high-intensity trials. This differential fatigue-related sensitivity decrease selectively enhanced the impact of criterion down-shifts on low-intensity trials, revealing how the interplay of two perceptual mechanisms and their modulation by fatigue combine to produce the observed overall pattern of asymmetric performance adjustments to varying visual intensity in continuous speeded detection. Our results have implications for similar patterns of sequential demand adaptation in other cognitive domains as well as for real-world prolonged detection performance.