Racial group membership is associated to gaze-mediated orienting in Italy

Viewing a face with averted gaze results in a spatial shift of attention in the corresponding direction, a phenomenon defined as gaze-mediated orienting. In the present paper, we investigated whether this effect is influenced by social factors. Across three experiments, White and Black participants were presented with faces of White and Black individuals. A modified spatial cueing paradigm was used in which a peripheral target stimulus requiring a discrimination response was preceded by a noninformative gaze cue. Results showed that Black participants shifted attention to the averted gaze of both ingroup and outgroup faces, whereas White participants selectively shifted attention only in response to individuals of their same group. Interestingly, the modulatory effect of social factors was context-dependent and emerged only when group membership was situationally salient to participants. It was hypothesized that differences in the relative social status of the two groups might account for the observed asymmetry between White and Black participants. A final experiment ruled out an alternative explanation based on differences in perceptual familiarity with the face stimuli. Overall, these findings strengthen the idea that gaze-mediated orienting is a socially-connoted phenomenon.     

Familiarity accentuates gaze cuing in women but not men

Gaze cuing, the tendency to shift attention in the direction other individuals are looking, is hypothesized to depend on a distinct neural module. One expectation of such a module is that information processing should be encapsulated within it. Here, we tested whether familiarity, a type of social knowledge, penetrates the neural circuits governing gaze cuing. Male and female subjects viewed the face of an adult male looking left or right and then pressed a keypad to indicate the location of a target appearing randomly left or right. Responses were faster for targets congruent with gaze direction. Moreover, gaze cuing was stronger in females than males. Contrary to the modularity hypothesis, familiarity enhanced gaze cuing, but only in females. Sex differences in the effects of familiarity on gaze cuing may reflect greater adaptive significance of social information for females than males.     

Gender and Facial Dominance in Gaze Cuing: Emotional Context Matters in the Eyes That We Follow

Gaze following is a socio-cognitive process that provides adaptive information about potential threats and opportunities in the individual’s environment. The aim of the present study was to investigate the potential interaction between emotional context and facial dominance in gaze following. We used the gaze cue task to induce attention to or away from the location of a target stimulus. In the experiment, the gaze cue either belonged to a (dominant looking) male face or a (non-dominant looking) female face. Critically, prior to the task, individuals were primed with pictures of threat or no threat to induce either a dangerous or safe environment. Findings revealed that the primed emotional context critically influenced the gaze cuing effect. While a gaze cue of the dominant male face influenced performance in both the threat and no-threat conditions, the gaze cue of the non-dominant female face only influenced performance in the no-threat condition. This research suggests an implicit, context-dependent follower bias, which carries implications for research on visual attention, social cognition, and leadership.     

I See What You Mean: How Attentional Selection Is Shaped by Ascribing Intentions to Others

The ability to understand and predict others’ behavior is essential for successful interactions. When making predictions about what other humans will do, we treat them as intentional systems and adopt the intentional stance, i.e., refer to their mental states such as desires and intentions. In the present experiments, we investigated whether the mere belief that the observed agent is an intentional system influences basic social attention mechanisms. We presented pictures of a human and a robot face in a gaze cuing paradigm and manipulated the likelihood of adopting the intentional stance by instruction: in some conditions, participants were told that they were observing a human or a robot, in others, that they were observing a human-like mannequin or a robot whose eyes were controlled by a human. In conditions in which participants were made to believe they were observing human behavior (intentional stance likely) gaze cuing effects were significantly larger as compared to conditions when adopting the intentional stance was less likely. This effect was independent of whether a human or a robot face was presented. Therefore, we conclude that adopting the intentional stance when observing others’ behavior fundamentally influences basic mechanisms of social attention. The present results provide striking evidence that high-level cognitive processes, such as beliefs, modulate bottom-up mechanisms of attentional selection in a top-down manner.     

Cues for early social skills: direct gaze modulates newborns' recognition of talking faces

Previous studies showed that, from birth, speech and eye gaze are two important cues in guiding early face processing and social cognition. These studies tested the role of each cue independently; however, infants normally perceive speech and eye gaze together. Using a familiarization-test procedure, we first familiarized newborn infants (n = 24) with videos of unfamiliar talking faces with either direct gaze or averted gaze. Newborns were then tested with photographs of the previously seen face and of a new one. The newborns looked longer at the face that previously talked to them, but only in the direct gaze condition. These results highlight the importance of both speech and eye gaze as socio-communicative cues by which infants identify others. They suggest that gaze and infant-directed speech, experienced together, are powerful cues for the development of early social skills.     

Facial-expression and gaze-selective responses in the monkey amygdala

The social behavior of both human and nonhuman primates relies on specializations for the recognition of individuals, their facial expressions, and their direction of gaze. A broad network of cortical and subcortical structures has been implicated in face processing, yet it is unclear whether co-occurring dimensions of face stimuli, such as expression and direction of gaze, are processed jointly or independently by anatomically and functionally segregated neural structures. Awake macaques were presented with a set of monkey faces displaying aggressive, neutral, and appeasing expressions with head and eyes either averted or directed. BOLD responses to these faces as compared to Fourier-phase-scrambled images revealed widespread activation of the superior temporal sulcus and inferotemporal cortex and included activity in the amygdala. The different dimensions of the face stimuli elicited distinct activation patterns among the amygdaloid nuclei. The basolateral amygdala, including the lateral, basal, and accessory basal nuclei, produced a stronger response for threatening than appeasing expressions. The central nucleus and bed nucleus of the stria terminalis responded more to averted than directed-gaze faces. Independent behavioral measures confirmed that faces with averted gaze were more arousing, suggesting the activity in the central nucleus may be related to attention and arousal.     

眼睛注视线索对物体认知加工的影响及其机制

眼睛注视作为一种重要的非语言社会线索，不仅可以传达他人丰富的注意方向信息，并且能够诱发独特的社会性注意行为. 近年来，研究者利用改编的社会性注意任务发现，眼睛注视线索还可以进一步影响我们对各种不同种类物体（用具、符号、面孔等）的感知觉加工，以及主观评价、记忆等其他高级认知加工过程. 眼睛注视线索对物体加工的这种影响受到诸多因素的调节，如面孔属性、数量以及注视模式等. 特别地，眼睛注视线索对物体加工的这一调制作用能够在无意识水平发生，具有一定的特异性. 此外，针对这一调制作用背后机制的研究暗示心理理论和观点采择可能参与其中，但仍有待进一步探究. 眼睛注视对物体加工影响的研究有助于我们深入理解社会互动的方式以及人类与环境的交互过程，因此具有重要的理论意义和社会应用价值.     

Intergroup threat gates social attention in humans

Humans shift their attention to follow another person''s gaze direction, a phenomenon called gaze cueing. This study examined whether a particular social factor, intergroup threat, modulates gaze cueing. As expected, stronger responses of a particular in-group to a threatening out-group were observed when the in-group, conditioned to perceive threat from one of two out-groups, was presented with facial stimuli from the threatening and non-threatening out-groups. These results suggest that intergroup threat plays an important role in shaping social attention. Furthermore, larger gaze-cueing effects were found for threatening out-group faces than for in-group faces only at the 200 ms but not the 800 ms stimulus onset asynchrony (SOA); the specificity of the gaze-cueing effects at the short SOA suggests that threat cues modulate the involuntary component of gaze cueing.     

The Impact of Perceived Social Power and Dangerous Context on Social Attention

Past research has shown that position in a social hierarchy modulates one''s social attention, as in the gaze cueing effect. While studies have manipulated the social status of others with whom the participants interact, we believe that a sense of one''s own social power is also a crucial factor affecting gaze following. In two experiments, we primed the social power of participants, using different approaches, to investigate the participants'' performance in a subsequent gaze cueing task. The results of Experiment 1 showed a stronger gaze cueing effect among participants who were primed with low social power, compared to those primed with high social power. Our predicted gender difference (i.e., women showing a stronger gaze cueing effect than men) was confirmed and this effect was found to be dominated by the lower social power condition. Experiment 2 manipulated the level of danger in the context and replicated the joint impact of gender and one''s perceived social power on gaze cueing effect, especially in the low danger context, in comparison to the high danger context. These findings demonstrate that one''s perceived social power has a concerted effect on social attention evoked by gaze, along with other factors such as gender and characteristics of the environment, and suggest the importance of further research on the complex relationship between an individual''s position in the social hierarchy and social attention.     

Social orienting in gaze leading: a mechanism for shared attention

Here, we report a novel social orienting response that occurs after viewing averted gaze. We show, in three experiments, that when a person looks from one location to an object, attention then shifts towards the face of an individual who has subsequently followed the person''s gaze to that same object. That is, contrary to ‘gaze following’, attention instead orients in the opposite direction to observed gaze and towards the gazing face. The magnitude of attentional orienting towards a face that ‘follows’ the participant''s gaze is also associated with self-reported autism-like traits. We propose that this gaze leading phenomenon implies the existence of a mechanism in the human social cognitive system for detecting when one''s gaze has been followed, in order to establish ‘shared attention’ and maintain the ongoing interaction.     

Social Interactions through the Eyes of Macaques and Humans

Group-living primates frequently interact with each other to maintain social bonds as well as to compete for valuable resources. Observing such social interactions between group members provides individuals with essential information (e.g. on the fighting ability or altruistic attitude of group companions) to guide their social tactics and choice of social partners. This process requires individuals to selectively attend to the most informative content within a social scene. It is unclear how non-human primates allocate attention to social interactions in different contexts, and whether they share similar patterns of social attention to humans. Here we compared the gaze behaviour of rhesus macaques and humans when free-viewing the same set of naturalistic images. The images contained positive or negative social interactions between two conspecifics of different phylogenetic distance from the observer; i.e. affiliation or aggression exchanged by two humans, rhesus macaques, Barbary macaques, baboons or lions. Monkeys directed a variable amount of gaze at the two conspecific individuals in the images according to their roles in the interaction (i.e. giver or receiver of affiliation/aggression). Their gaze distribution to non-conspecific individuals was systematically varied according to the viewed species and the nature of interactions, suggesting a contribution of both prior experience and innate bias in guiding social attention. Furthermore, the monkeys’ gaze behavior was qualitatively similar to that of humans, especially when viewing negative interactions. Detailed analysis revealed that both species directed more gaze at the face than the body region when inspecting individuals, and attended more to the body region in negative than in positive social interactions. Our study suggests that monkeys and humans share a similar pattern of role-sensitive, species- and context-dependent social attention, implying a homologous cognitive mechanism of social attention between rhesus macaques and humans.     

Perception of Social Cues of Danger in Autism Spectrum Disorders

Intuitive grasping of the meaning of subtle social cues is particularly affected in autism spectrum disorders (ASD). Despite their relevance in social communication, the effect of averted gaze in fearful faces in conveying a signal of environmental threat has not been investigated using real face stimuli in adults with ASD. Here, using functional MRI, we show that briefly presented fearful faces with averted gaze, previously shown to be a strong communicative signal of environmental danger, produce different patterns of brain activation than fearful faces with direct gaze in a group of 26 normally intelligent adults with ASD compared with 26 matched controls. While implicit cue of threat produces brain activation in attention, emotion processing and mental state attribution networks in controls, this effect is absent in individuals with ASD. Instead, individuals with ASD show activation in the subcortical face-processing system in response to direct eye contact. An effect of differences in looking behavior was excluded in a separate eye tracking experiment. Our data suggest that individuals with ASD are more sensitive to direct eye contact than to social signals of danger conveyed by averted fearful gaze.     

Evidence for adaptive design in human gaze preference

Many studies have investigated the physical cues that influence face preferences. By contrast, relatively few studies have investigated the effects of facial cues to the direction and valence of others' social interest (i.e. gaze direction and facial expressions) on face preferences. Here we found that participants demonstrated stronger preferences for direct gaze when judging the attractiveness of happy faces than that of disgusted faces, and that this effect of expression on the strength of attraction to direct gaze was particularly pronounced for judgements of opposite-sex faces (study 1). By contrast, no such opposite-sex bias in preferences for direct gaze was observed when participants judged the same faces for likeability (study 2). Collectively, these findings for a context-sensitive opposite-sex bias in preferences for perceiver-directed smiles, but not perceiver-directed disgust, suggest gaze preference functions, at least in part, to facilitate efficient allocation of mating effort, and evince adaptive design in the perceptual mechanisms that underpin face preferences.     

Perceptual and Gaze Biases during Face Processing: Related or Not?

Previous studies have demonstrated a left perceptual bias while looking at faces, due to the fact that observers mainly use information from the left side of a face (from the observer''s point of view) to perform a judgment task. Such a bias is consistent with the right hemisphere dominance for face processing and has sometimes been linked to a left gaze bias, i.e. more and/or longer fixations on the left side of the face. Here, we recorded eye-movements, in two different experiments during a gender judgment task, using normal and chimeric faces which were presented above, below, right or left to the central fixation point or on it (central position). Participants performed the judgment task by remaining fixated on the fixation point or after executing several saccades (up to three). A left perceptual bias was not systematically found as it depended on the number of allowed saccades and face position. Moreover, the gaze bias clearly depended on the face position as the initial fixation was guided by face position and landed on the closest half-face, toward the center of gravity of the face. The analysis of the subsequent fixations revealed that observers move their eyes from one side to the other. More importantly, no apparent link between gaze and perceptual biases was found here. This implies that we do not look necessarily toward the side of the face that we use to make a gender judgment task. Despite the fact that these results may be limited by the absence of perceptual and gaze biases in some conditions, we emphasized the inter-individual differences observed in terms of perceptual bias, hinting at the importance of performing individual analysis and drawing attention to the influence of the method used to study this bias.     

Race Guides Attention in Visual Search

It is known that faces are rapidly and even unconsciously categorized into social groups (black vs. white, male vs. female). Here, I test whether preferences for specific social groups guide attention, using a visual search paradigm. In Experiment 1 participants searched displays of neutral faces for an angry or frightened target face. Black target faces were detected more efficiently than white targets, indicating that black faces attracted more attention. Experiment 2 showed that attention differences between black and white faces were correlated with individual differences in automatic race preference. In Experiment 3, using happy target faces, the attentional preference for black over white faces was eliminated. Taken together, these results suggest that automatic preferences for social groups guide attention to individuals from negatively valenced groups, when people are searching for a negative emotion such as anger or fear.     

Neural Signals Evoked by Stimuli of Increasing Social Scene Complexity Are Detectable at the Single-Trial Level and Right Lateralized

Classification of neural signals at the single-trial level and the study of their relevance in affective and cognitive neuroscience are still in their infancy. Here we investigated the neurophysiological correlates of conditions of increasing social scene complexity using 3D human models as targets of attention, which may also be important in autism research. Challenging single-trial statistical classification of EEG neural signals was attempted for detection of oddball stimuli with increasing social scene complexity. Stimuli had an oddball structure and were as follows: 1) flashed schematic eyes, 2) simple 3D faces flashed between averted and non-averted gaze (only eye position changing), 3) simple 3D faces flashed between averted and non-averted gaze (head and eye position changing), 4) animated avatar alternated its gaze direction to the left and to the right (head and eye position), 5) environment with 4 animated avatars all of which change gaze and one of which is the target of attention. We found a late (> 300 ms) neurophysiological oddball correlate for all conditions irrespective of their complexity as assessed by repeated measures ANOVA. We attempted single-trial detection of this signal with automatic classifiers and obtained a significant balanced accuracy classification of around 79%, which is noteworthy given the amount of scene complexity. Lateralization analysis showed a specific right lateralization only for more complex realistic social scenes. In sum, complex ecological animations with social content elicit neurophysiological events which can be characterized even at the single-trial level. These signals are right lateralized. These finding paves the way for neuroscientific studies in affective neuroscience based on complex social scenes, and given the detectability at the single trial level this suggests the feasibility of brain computer interfaces that can be applied to social cognition disorders such as autism.     

Natural gaze signaling in a social context

Evolutionary theory, augmented by a vast literature on gaze cuing and gaze following, suggests that the unique high-contrast morphology of the human eye evolved for rapid and silent communication between conspecifics. While this theory rests on the fundamental idea that humans use their eyes to signal information, empirical studies have focused exclusively on the effects of gaze cues on human receivers. In a series of three experiments we examined the other side of the communication dynamic by investigating if, and when, humans signal gaze information to other humans in a natural, but controlled, situation involving food consumption. First, we established that there is a normative behavior to look away when someone begins to bite. Second, we found that participants were significantly more likely to look down at their food before taking a bite when they were eating with another person versus alone. Lastly, we found that in pairs where a social connection has been established, when one person looks down signaling that a bite is forthcoming, the other person tends to look away. These results demonstrate that natural gaze signaling occurs in the context of eating, and it can, dependent on the relationship between the pair, trigger a gaze response that is different from gaze following. Our study shows that natural social attention between individuals is a two-way street, where each person can signal and read gaze information, consistent with the idea that human eye morphology evolved to facilitate communication between conspecifics.     

Loneliness and Hypervigilance to Social Cues in Females: An Eye-Tracking Study

The goal of the present study was to examine whether lonely individuals differ from nonlonely individuals in their overt visual attention to social cues. Previous studies showed that loneliness was related to biased post-attentive processing of social cues (e.g., negative interpretation bias), but research on whether lonely and nonlonely individuals also show differences in an earlier information processing stage (gazing behavior) is very limited. A sample of 25 lonely and 25 nonlonely students took part in an eye-tracking study consisting of four tasks. We measured gazing (duration, number of fixations and first fixation) at the eyes, nose and mouth region of faces expressing emotions (Task 1), at emotion quadrants (anger, fear, happiness and neutral expression) (Task 2), at quadrants with positive and negative social and nonsocial images (Task 3), and at the facial area of actors in video clips with positive and negative content (Task 4). In general, participants tended to gaze most often and longest at areas that conveyed most social information, such as the eye region of the face (T1), and social images (T3). Participants gazed most often and longest at happy faces (T2) in still images, and more often and longer at the facial area in negative than in positive video clips (T4). No differences occurred between lonely and nonlonely participants in their gazing times and frequencies, nor at first fixations at social cues in the four different tasks. Based on this study, we found no evidence that overt visual attention to social cues differs between lonely and nonlonely individuals. This implies that biases in social information processing of lonely individuals may be limited to other phases of social information processing. Alternatively, biased overt attention to social cues may only occur under specific conditions, for specific stimuli or for specific lonely individuals.     

Evidence that emotion mediates social attention in rhesus macaques

Background

Recent work on non-human primates indicates that the allocation of social attention is mediated by characteristics of the attending animal, such as social status and genotype, as well as by the value of the target to which attention is directed. Studies of humans indicate that an individual’s emotion state also plays a crucial role in mediating their social attention; for example, individuals look for longer towards aggressive faces when they are feeling more anxious, and this bias leads to increased negative arousal and distraction from other ongoing tasks. To our knowledge, no studies have tested for an effect of emotion state on allocation of social attention in any non-human species.

Methodology

We presented captive adult male rhesus macaques with pairs of adult male conspecific face images - one with an aggressive expression, one with a neutral expression - and recorded gaze towards these images. Each animal was tested twice, once during a putatively stressful condition (i.e. following a veterinary health check), and once during a neutral (or potentially positive) condition (i.e. a period of environmental enrichment). Initial analyses revealed that behavioural indicators of anxiety and stress were significantly higher after the health check than during enrichment, indicating that the former caused a negative shift in emotional state.

Principle Findings

The macaques showed initial vigilance for aggressive faces across both conditions, but subsequent responses differed between conditions. Following the health check, initial vigilance was followed by rapid and sustained avoidance of aggressive faces. By contrast, during the period of enrichment, the macaques showed sustained attention towards the same aggressive faces.

Conclusions/Significance

These data provide, to our knowledge, the first evidence that shifts in emotion state mediate social attention towards and away from facial cues of emotion in a non-human animal. This work provides novel insights into the evolution of emotion-attention interactions in humans, and mechanisms of social behaviour in non-human primates, and may have important implications for understanding animal psychological wellbeing.