Age differences in neural activity related to mentalizing during person perception

ABSTRACT

Mentalizing, or thinking about others’ mental states, shapes social interactions. Older adults (OA) have reduced mentalizing capacities reflected by lower medial prefrontal cortex (mPFC) activation. The current study assessed if OA’ lower mPFC activation reflects less spontaneous mentalizing during person perception. Younger adults (YA) and OA viewed ingroup White and outgroup Black and Asian faces and completed a mentalizing task during fMRI. Afterward, they completed a task in which they inferred mental states from faces. Using an mPFC region defined by the mentalizing task, OA had lower activity than YA during person perception. OA’ mPFC activity toward faces positively related to their mentalizing outside the scanner. The extent of OA’ lower mPFC activation during person perception may depend on their actual detection of mental states in faces. Further, YA’, but not OA’, mPFC activity distinguished between outgroups. OA’ lower mentalizing-related mPFC activity may reduce their ability to individuate outgroup members.     

“Avoiding or approaching eyes”? Introversion/extraversion affects the gaze-cueing effect

We investigated whether the extra-/introversion personality dimension can influence processing of others’ eye gaze direction and emotional facial expression during a target detection task. On the basis of previous evidence showing that self-reported trait anxiety can affect gaze-cueing with emotional faces, we also verified whether trait anxiety can modulate the influence of intro-/extraversion on behavioral performance. Fearful, happy, angry or neutral faces, with either direct or averted gaze, were presented before the target appeared in spatial locations congruent or incongruent with stimuli’s eye gaze direction. Results showed a significant influence of intra-/extraversion dimension on gaze-cueing effect for angry, happy, and neutral faces with averted gaze. Introverts did not show the gaze congruency effect when viewing angry expressions, but did so with happy and neutral faces; extraverts showed the opposite pattern. Importantly, the influence of intro-/extraversion on gaze-cueing was not mediated by trait anxiety. These findings demonstrated that personality differences can shape processing of interactions between relevant social signals.     

Modulation of reflexive orienting to gaze direction by facial expressions

Facial expression and gaze perception are thought to share brain mechanisms but behavioural interactions, especially from gaze-cueing paradigms, are inconsistent. We conducted a series of gaze-cueing studies using dynamic facial cues to examine orienting across different emotional expression and task conditions, including face inversion. Across experiments, at a short stimulus–onset asynchrony (SOA) we observed both an expression effect (i.e., faster responses when the face was emotional versus neutral) and a cue validity effect (i.e., faster responses when the target was gazed-at), but no interaction between validity and emotion. Results from face inversion suggest that the emotion effect may have been due to both facial expression and stimulus motion. At longer SOAs, validity and emotion interacted such that cueing by emotional faces, fearful faces in particular, was enhanced relative to neutral faces. These results converge with a growing body of evidence that suggests that gaze and expression are initially processed independently and interact at later stages to direct attentional orienting.     

Responding to the direction of the eyes: In search of the masked gaze-cueing effect

Recent studies have demonstrated that masked gaze cues can produce a cueing effect. Those studies, however, all utilized a localization task and, hence, are ambiguous with respect to whether the previously observed masked gaze-cueing effect reflects the orienting of attention or the preparation of a motor response. The aim of the present study was to investigate this issue by determining whether masked gaze cues can modulate responses in detection and discrimination tasks, both of which isolate spatial attention from response priming. First, we found a gaze-cueing effect for unmasked cues in detection, discrimination, and localization tasks, which suggests that the gaze-cueing effect for visible cues is not task dependent. Second, and in contrast, we found a gaze-cueing effect for masked cues in a localization task, but not in detection or discrimination tasks, which suggests that the gaze-cueing effect for masked cues is task dependent. Therefore, the present study shows that the masked gaze-cueing effect is attributed to response priming, as opposed to the orienting of spatial attention.     

The appeal of the devil’s eye: social evaluation affects social attention

Humans typically exhibit a tendency to follow the gaze of conspecifics, a social attention behaviour known as gaze cueing. Here, we addressed whether episodically learned social knowledge about the behaviours performed by the individual bearing the gaze can influence this phenomenon. In a learning phase, different faces were systematically associated with either positive or negative behaviours. The same faces were then used as stimuli in a gaze-cueing task. The results showed that faces associated with antisocial norm-violating behaviours triggered stronger gaze-cueing effects as compared to faces associated with sociable behaviours. Importantly, this was especially evident for participants who perceived the presented norm-violating behaviours as far more negative as compared to positive behaviours. These findings suggest that reflexive attentional responses can be affected by our appraisal of the valence of the behaviours of individuals around us.     

Face in profile view reduces perceived facial expression intensity: An eye-tracking study

Recent studies measuring the facial expressions of emotion have focused primarily on the perception of frontal face images. As we frequently encounter expressive faces from different viewing angles, having a mechanism which allows invariant expression perception would be advantageous to our social interactions. Although a couple of studies have indicated comparable expression categorization accuracy across viewpoints, it is unknown how perceived expression intensity and associated gaze behaviour change across viewing angles. Differences could arise because diagnostic cues from local facial features for decoding expressions could vary with viewpoints. Here we manipulated orientation of faces (frontal, mid-profile, and profile view) displaying six common facial expressions of emotion, and measured participants' expression categorization accuracy, perceived expression intensity and associated gaze patterns. In comparison with frontal faces, profile faces slightly reduced identification rates for disgust and sad expressions, but significantly decreased perceived intensity for all tested expressions. Although quantitatively viewpoint had expression-specific influence on the proportion of fixations directed at local facial features, the qualitative gaze distribution within facial features (e.g., the eyes tended to attract the highest proportion of fixations, followed by the nose and then the mouth region) was independent of viewpoint and expression type. Our results suggest that the viewpoint-invariant facial expression processing is categorical perception, which could be linked to a viewpoint-invariant holistic gaze strategy for extracting expressive facial cues.     

A fMRI study of word retrieval in aphasia

The neural mechanisms underlying recovery of cognitive functions are incompletely understood. Aim of this study was to assess, using functional magnetic resonance (fMRI), the pattern of brain activity during covert word retrieval to letter and semantic cues in five aphasic patients after stroke, in order to assess the modifications of brain function which may be related to recovery. Four out of five patients had undergone language recovery, according to standard testing, after at least 6 months of rehabilitation. The cerebral activation of each patient was evaluated and compared with the activation pattern of normal controls studied with the same fMRI paradigm. In the patients, the pattern of brain activation was influenced by the site and extent of the lesion, by the degree of recovery of language, as reflected by task performance outside the scanner, and by task requirements. In the case of word retrieval to letter cues, a good performance was directly related to the activation in Broca's area, or in the right-sided homologue. On the other hand, in the case of semantic fluency, the relationship between performance level and activation was less clear-cut, because of extensive recruitment of frontal areas in patients with defective performance. These findings suggest that the performance in letter fluency is dependent on the integrity of the left inferior frontal cortex, with the participation of the homologous right hemispheric region when the left inferior frontal cortex is entirely of partially damaged. Semantic fluency, which engages the distributed network of semantic memory, is also associated with more extensive patterns of cerebral activation, which however appear to reflect retrieval effort rather than retrieval success.     

Look into my eyes: gaze direction and person memory

The current research considered the effects of gaze direction on a fundamental aspect of social cogition: person memory. It was anticipated that a person's direction of gaze (i.e., direct or averted) would impact his or her subsequent memorability, such that recognition would be enhanced for targets previously displaying direct gaze. In Experiment 1, participants were presented with faces displaying either direct or averted gaze in a person-classification (i.e., conceptual) task. Then, in a surprise memory test, they were required to report whether a presented face had been seen before. As expected, a recognition advantage was observed for targets displaying direct gaze during the initial classification task. This finding was replicated and extended in a second experiment in which participants initially reported the spatial location (i.e., perceptual task) of each face. We consider the implications of these findings for basic aspects of social-cognitive functioning and person perception.     

Effects of perceived mutual gaze and gender on face processing and recognition memory

Perceived gaze contact in seen faces may convey important social signals. We examined whether gaze perception affects face processing during two tasks: Online gender judgement, and later incidental recognition memory. Individual faces were presented with eyes directed either straight towards the viewer or away, while these faces were seen in either frontal or three-quarters view. Participants were slower to make gender judgements for faces with direct versus averted eye gaze, but this effect was particularly pronounced for faces with opposite gender to the observer, and seen in three-quarters view. During subsequent surprise recognition-memory testing, recognition was better for faces previously seen with direct than averted gaze, again especially for the opposite gender to the observer. The effect of direct gaze was stronger in both tasks when the head was seen in three-quarters rather than in frontal view, consistent with the greater salience of perceived eye contact for deviated faces. However, in the memory test, face recognition was also relatively enhanced for faces of opposite gender in front views when their gaze was averted rather than direct. Together, these results indicate that perceived eye contact can interact with facial processing during gender judgements and recognition memory, even when gaze direction is task-irrelevant, and particularly for faces of opposite gender to the observer (an influence which controls for stimulus factors when considering observers of both genders). These findings appear consistent with recent neuroimaging evidence that social facial cues can modulate visual processing in cortical regions involved in face processing and memory, presumably via interconnections with brain systems specialized for gaze perception and social monitoring.     

Social attention across borders: A cross-cultural investigation of gaze cueing elicited by same- and other-ethnicity faces

The gaze-cueing effect is a robust phenomenon which illustrates how attention can be shaped by social factors. In four experiments, the present study explored the interaction between the ethnic membership of the participant and that of the face providing the gaze cue. Firstly, we aimed to further investigate the differential impact of White, Black, and Asian faces on the gaze-cueing effect in White individuals. Secondly, we aimed to explore, for the first time, the impact of faces belonging to different ethnicities on gaze cueing in Chinese participants. The results allowed to rule out alternative accounts and showed that White participants exhibit a gaze-cueing effect for White and Asian faces, but not for Black faces, consistent with previous studies. As regards Chinese participants, the overall findings suggested a stronger gaze-cueing effect for White faces than for Asian faces. The results are discussed with reference to differences in the perceived social status of the various groups, pointing to the need of taking into account different cultural contexts.     

Neural recruitment related to threat perception differs as a function of adolescent sleep

Detecting threat cues in the environment is an important aspect of social functioning. This is particularly true for adolescents as social threats become more salient and they navigate increasingly complex relationships outside of the family. Sleep relates to socioemotional processing throughout development, but the neurobiological relevance of sleep for threat perceptions in adolescence remains unknown. In the present study, 46 human adolescents (aged 14–18 years; 26 female) made judgments while undergoing a brain scan about whether unfamiliar, affectively neutral, computer‐generated faces were threatening. Prior to the scan, several indices of sleep were assessed nightly for two‐weeks using actigraphy. Sleep duration and poor sleep quality (defined as less efficiency, more awakenings, longer awakenings), factors influenced by biological and psychosocial changes during adolescence, elicited distinct neural activation patterns. Sleep duration was positively associated with activation in visual and face processing regions (occipital cortex, occipital fusiform gyrus), and this activation was linked to increased threat detection during the threat perception task. Sleep quality was negatively related to dorsolateral prefrontal cortex activation, which moderated the relation between reaction time (RT) and exposure to faces. Findings suggest reduced threat perception for adolescents with shorter sleep durations and more impulsive responding (as evinced by less consistent RT) for adolescents experiencing worse quality sleep. This study identifies an association between sleep and neural functioning relevant for socioemotional decision making during adolescence, a time when these systems undergo significant development.     

线索类型对阈下注视线索效应的影响

实验结合连续闪烁抑制范式和线索化范式, 通过操纵直视面孔和斜视面孔的呈现方式, 考察了动静线索类型对注视线索效应的影响。结果表明：两种线索在阈上条件都能产生注视线索效应, 且动态线索诱发的效应更大; 无意识条件下有且仅有动态注视线索能诱发注视线索效应。这说明眼睛运动是产生阈下注视线索效应的必要条件; 眼睛运动会增强阈上注视线索效应, 静态注视线索效应依赖于意识。研究结果支持了社会知觉与心理理论交互模型。     

Physical self-similarity enhances the gaze-cueing effect

Important social information can be gathered from the direction of another person's gaze, such as their intentions and aspects of the environment that are relevant to those intentions. Previous work has examined the effect of gaze on attention through the gaze-cueing effect: an enhancement of performance in detecting targets that appear where another person is looking. The present study investigated whether the physical self-similarity of a face could increase its impact on attention. Self-similarity was manipulated by morphing participants' faces with those of strangers. The effect of gaze direction on target detection was strongest for faces morphed with the participant's face. The results support previous work suggesting that self-similar faces are processed differently from dissimilar faces. The data also demonstrate that a face's similarity to one's own face influences the degree to which that face guides our attention in the environment.     

Face-to-face interference in typical and atypical development

Visual communication cues facilitate interpersonal communication. It is important that we look at faces to retrieve and subsequently process such cues. It is also important that we sometimes look away from faces as they increase cognitive load that may interfere with online processing. Indeed, when typically developing individuals hold face gaze it interferes with task completion. In this novel study we quantify face interference for the first time in Williams syndrome (WS) and Autism Spectrum Disorder (ASD). These disorders of development impact on cognition and social attention, but how do faces interfere with cognitive processing? Individuals developing typically as well as those with ASD (n = 19) and WS (n = 16) were recorded during a question and answer session that involved mathematics questions. In phase 1 gaze behaviour was not manipulated, but in phase 2 participants were required to maintain eye contact with the experimenter at all times. Looking at faces decreased task accuracy for individuals who were developing typically. Critically, the same pattern was seen in WS and ASD, whereby task performance decreased when participants were required to hold face gaze. The results show that looking at faces interferes with task performance in all groups. This finding requires the caveat that individuals with WS and ASD found it harder than individuals who were developing typically to maintain eye contact throughout the interaction. Individuals with ASD struggled to hold eye contact at all points of the interaction while those with WS found it especially difficult when thinking.     

Affective evaluations of objects are influenced by observed gaze direction and emotional expression

Gaze direction signals another person's focus of interest. Facial expressions convey information about their mental state. Appropriate responses to these signals should reflect their combined influence, yet current evidence suggests that gaze-cueing effects for objects near an observed face are not modulated by its emotional expression. Here, we extend the investigation of perceived gaze direction and emotional expression by considering their combined influence on affective judgments. While traditional response-time measures revealed equal gaze-cueing effects for happy and disgust faces, affective evaluations critically depended on the combined product of gaze and emotion. Target objects looked at with a happy expression were liked more than objects looked at with a disgust expression. Objects not looked at were rated equally for both expressions. Our results demonstrate that facial expression does modulate the way that observers utilize gaze cues: Objects attended by others are evaluated according to the valence of their facial expression.     

Trying to trust: Brain activity during interpersonal social attitude change

Interpersonal trust and distrust are important components of human social interaction. Although several studies have shown that brain function is associated with either trusting or distrusting others, very little is known regarding brain function during the control of social attitudes, including trust and distrust. This study was designed to investigate the neural mechanisms involved when people attempt to control their attitudes of trust or distrust toward another person. We used a novel control-of-attitudes fMRI task, which involved explicit instructions to control attitudes of interpersonal trust and distrust. Control of trust or distrust was operationally defined as changes in trustworthiness evaluations of neutral faces before and after the control-of-attitudes fMRI task. Overall, participants (n = 60) evaluated faces paired with the distrust instruction as being less trustworthy than faces paired with the trust instruction following the control-of-distrust task. Within the brain, both the control-of-trust and control-of-distrust conditions were associated with increased temporoparietal junction, precuneus (PrC), inferior frontal gyrus (IFG), and medial prefrontal cortex activity. Individual differences in the control of trust were associated with PrC activity, and individual differences in the control of distrust were associated with IFG activity. Together, these findings identify a brain network involved in the explicit control of distrust and trust and indicate that the PrC and IFG may serve to consolidate interpersonal social attitudes.     

Ventromedial prefrontal-subcortical systems and the generation of affective meaning

The ventromedial prefrontal cortex (vmPFC) comprises a set of interconnected regions that integrate information from affective sensory and social cues, long-term memory, and representations of the 'self'. Alhough the vmPFC is implicated in a variety of seemingly disparate processes, these processes are organized around a common theme. The vmPFC is not necessary for affective responses per se, but is critical when affective responses are shaped by conceptual information about specific outcomes. The vmPFC thus functions as a hub that links concepts with brainstem systems capable of coordinating organism-wide emotional behavior, a process we describe in terms of the generation of affective meaning, and which could explain the common role played by the vmPFC in a range of experimental paradigms.     

Role of the hippocampus and orbitofrontal cortex during the disambiguation of social cues in working memory

Human social interactions are complex behaviors requiring the concerted effort of multiple neural systems to track and monitor the individuals around us. Cognitively, adjusting our behavior on the basis of changing social cues such as facial expressions relies on working memory and the ability to disambiguate, or separate, the representations of overlapping stimuli resulting from viewing the same individual with different facial expressions. We conducted an fMRI experiment examining the brain regions contributing to the encoding, maintenance, and retrieval of overlapping identity information during working memory using a delayed match-to-sample task. In the overlapping condition, two faces from the same individual with different facial expressions were presented at sample. In the nonoverlapping condition, the two sample faces were from two different individuals with different expressions. fMRI activity was assessed by contrasting the overlapping and nonoverlapping conditions at sample, delay, and test. The lateral orbitofrontal cortex showed increased fMRI signal in the overlapping condition in all three phases of the delayed match-to-sample task and increased functional connectivity with the hippocampus when encoding overlapping stimuli. The hippocampus showed increased fMRI signal at test. These data suggest that lateral orbitofrontal cortex helps encode and maintain representations of overlapping stimuli in working memory, whereas the orbitofrontal cortex and hippocampus contribute to the successful retrieval of overlapping stimuli. We suggest that the lateral orbitofrontal cortex and hippocampus play a role in encoding, maintaining, and retrieving social cues, especially when multiple interactions with an individual need to be disambiguated in a rapidly changing social context in order to make appropriate social responses.     

The amygdalostriatal and corticostriatal effective connectivity in anticipation and evaluation of facial attractiveness

Decision-making consists of several stages of information processing, including an anticipation stage and an outcome evaluation stage. Previous studies showed that the ventral striatum (VS) is pivotal to both stages, bridging motivation and action, and it works in concert with the ventral medial prefrontal cortex (vmPFC) and the amygdala. However, evidence concerning how the VS works together with the vmPFC and the amygdala came mainly from neuropathology and animal studies; little is known about the dynamics of this network in the functioning human brain. Here we used fMRI combined with dynamic causal modeling (DCM) to investigate the information flow along amygdalostriatal and corticostriatal pathways in a facial attractiveness guessing task. Specifically, we asked participants to guess whether a blurred photo of female face was attractive and to wait for a few seconds (“anticipation stage”) until an unblurred photo of feedback face, which was either attractive or unattractive, was presented (“outcome evaluation stage”). At the anticipation stage, the bilateral amygdala and VS showed higher activation for the “attractive” than for the “unattractive” guess. At the outcome evaluation stage, the vmPFC and the bilateral VS were more activated by feedback faces whose attractiveness was congruent with the initial guess than by incongruent faces; however, this effect was only significant for attractive faces, not for unattractive ones. DCM showed that at the anticipation stage, the choice-related information entered the amygdalostriatal pathway through the amygdala and was projected to the VS. At the evaluation stage, the outcome-related information entered the corticostriatal pathway through the vmPFC. Bidirectional connectivities existed between the vmPFC and VS, with the VS-to-vmPFC connectivity weakened by unattractive faces. These findings advanced our understanding of the reward circuitry by demonstrating the pattern of information flow along the amygdalostriatal and corticostriatal pathways at different stages of decision-making.     

The BOLD response during Stroop task-like inhibition paradigms: Effects of task difficulty and task-relevant modality

Previous studies of the Stroop task propose two key mediators: the prefrontal and cingulate cortices but hints exist of functional specialization within these regions. This study aimed to examine the effect of task modality upon the prefrontal and cingulate response by examining the response to colour, number, and shape Stroop tasks whilst BOLD fMRI images were acquired on a Siemens 3T MRI scanner. Behavioural analyses indicated facilitation and interference effects and a noticeable effect of task difficulty. Some modular effects of modality were observed in the prefrontal cortex that survived exclusion of task difficulty related activations. No effect of task-relevant information was observed in the anterior cingulate. Future comparisons of the mediation of selective attention need to consider the effects of task context and task difficulty.