Joint Attention without Gaze Following: Human Infants and Their Parents Coordinate Visual Attention to Objects through Eye-Hand Coordination

The coordination of visual attention among social partners is central to many components of human behavior and human development. Previous research has focused on one pathway to the coordination of looking behavior by social partners, gaze following. The extant evidence shows that even very young infants follow the direction of another''s gaze but they do so only in highly constrained spatial contexts because gaze direction is not a spatially precise cue as to the visual target and not easily used in spatially complex social interactions. Our findings, derived from the moment-to-moment tracking of eye gaze of one-year-olds and their parents as they actively played with toys, provide evidence for an alternative pathway, through the coordination of hands and eyes in goal-directed action. In goal-directed actions, the hands and eyes of the actor are tightly coordinated both temporally and spatially, and thus, in contexts including manual engagement with objects, hand movements and eye movements provide redundant information about where the eyes are looking. Our findings show that one-year-olds rarely look to the parent''s face and eyes in these contexts but rather infants and parents coordinate looking behavior without gaze following by attending to objects held by the self or the social partner. This pathway, through eye-hand coupling, leads to coordinated joint switches in visual attention and to an overall high rate of looking at the same object at the same time, and may be the dominant pathway through which physically active toddlers align their looking behavior with a social partner.     

Please Don't! The Automatic Extrapolation of Dangerous Intentions

Facial emotions and emotional body postures can easily grab attention in social communication. In the context of faces, gaze has been shown as an important cue for orienting attention, but less is known for other important body parts such as hands. In the present study we investigated whether hands may orient attention due to the emotional features they convey. By implying motion in static photographs of hands, we aimed at furnishing observers with information about the intention to act and at testing if this interacted with the hand automatic coding. In this study, we compared neutral and frontal hands to emotionally threatening hands, rotated along their radial-ulnar axes in a Sidedness task (a Simon-like task based on automatic access to body representation). Results showed a Sidedness effect for both the palm and the back views with either neutral and emotional hands. More important, no difference was found between the two views for neutral hands, but it emerged in the case of the emotional hands: faster reaction times were found for the palm than the back view. The difference was ascribed to palm views'' “offensive” pose: a source of threat that might have raised participants'' arousal. This hypothesis was also supported by conscious evaluations of the dimensions of valence (pleasant-unpleasant) and arousal. Results are discussed in light of emotional feature coding.     

Does the perception of moving eyes trigger reflexive visual orienting in autism?

Does movement of the eyes in one or another direction function as an automatic attentional cue to a location of interest? Two experiments explored the directional movement of the eyes in a full face for speed of detection of an aftercoming location target in young people with autism and in control participants. Our aim was to investigate whether a low-level perceptual impairment underlies the delay in gaze following characteristic of autism. The participants'' task was to detect a target appearing on the left or right of the screen either 100 ms or 800 ms after a face cue appeared with eyes averting to the left or right. Despite instructions to ignore eye-movement in the face cue, people with autism and control adolescents were quicker to detect targets that had been preceded by an eye movement cue congruent with target location compared with targets preceded by an incongruent eye movement cue. The attention shifts are thought to be reflexive because the cue was to be ignored, and because the effect was found even when cue-target duration was short (100 ms). Because (experiment two) the effect persisted even when the face was inverted, it would seem that the direction of movement of eyes can provide a powerful (involuntary) cue to a location.     

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.     

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.     

Beliefs about the Minds of Others Influence How We Process Sensory Information

Attending where others gaze is one of the most fundamental mechanisms of social cognition. The present study is the first to examine the impact of the attribution of mind to others on gaze-guided attentional orienting and its ERP correlates. Using a paradigm in which attention was guided to a location by the gaze of a centrally presented face, we manipulated participants'' beliefs about the gazer: gaze behavior was believed to result either from operations of a mind or from a machine. In Experiment 1, beliefs were manipulated by cue identity (human or robot), while in Experiment 2, cue identity (robot) remained identical across conditions and beliefs were manipulated solely via instruction, which was irrelevant to the task. ERP results and behavior showed that participants'' attention was guided by gaze only when gaze was believed to be controlled by a human. Specifically, the P1 was more enhanced for validly, relative to invalidly, cued targets only when participants believed the gaze behavior was the result of a mind, rather than of a machine. This shows that sensory gain control can be influenced by higher-order (task-irrelevant) beliefs about the observed scene. We propose a new interdisciplinary model of social attention, which integrates ideas from cognitive and social neuroscience, as well as philosophy in order to provide a framework for understanding a crucial aspect of how humans'' beliefs about the observed scene influence sensory processing.     

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.     

Young infants' neural processing of objects is affected by eye gaze direction and emotional expression

Eye gaze is an important social cue which is used to determine another person's focus of attention and intention to communicate. In combination with a fearful facial expression eye gaze can also signal threat in the environment. The ability to detect and understand others' social signals is essential in order to avoid danger and enable social evaluation. It has been a matter of debate when infants are able to use gaze cues and emotional facial expressions in reference to external objects. Here we demonstrate that by 3 months of age the infant brain differentially responds to objects as a function of how other people are reacting to them. Using event-related electrical brain potentials (ERPs), we show that an indicator of infants' attention is enhanced by an adult's expression of fear toward an unfamiliar object. The infant brain showed an increased Negative central (Nc) component toward objects that had been previously cued by an adult's eye gaze and frightened facial expression. Our results further suggest that infants' sensitivity cannot be due to a general arousal elicited by a frightened face with eye gaze directed at an object. The neural attention system of 3 month old infants is sensitive to an adult's eye gaze direction in combination with a fearful expression. This early capacity may lay the foundation for the development of more sophisticated social skills such as social referencing, language, and theory of mind.     

Environmental threat influences preferences for sexual dimorphism in male and female faces but not voices or dances

During evolution, humans faced the trade-off between preferences for feminine and masculine traits which are presumably connected to parental care, and genetic quality or provisioning abilities, respectively. Recent research has shown that environmental factors influence preferences for femininity/masculinity in potential mates. However, studies mainly focus on women's preferences for isolated cues in men. We examined the influence of pathogen and resource threat on women's and men's preference for femininity/masculinity in opposite sex unmanipulated faces, voices, and dances. Three hundred seventy (206 women) students, aged 18–35 years, from universities across the state of Sao Paulo, Brazil, were primed with newspaper-like articles on either pathogen threat (Aedes aegypti, and its mosquito-borne diseases) or resource threat (=economic crisis), and compared to a control-priming condition (lions poisoned in a Kenyan Reserve). Participants were randomly assigned to rate attractiveness of the stimuli in one of the mating strategies (i.e., short-term or long-term relationship context). After each priming article, participants rated attractiveness of pre-rated masculine and feminine stimuli of the opposite sex in a standalone-rating design. The environmental threats and the control-priming conditions were shown in a random sequence. We found that the environmental threat and the mating strategies had no systematic effect on preferences for faces, voices and behavior, suggesting that different modalities can cue to different individual qualities and can be used differently according to the environmental context and relationship strategy. The environmental threat only had a weak effect on preferences for facial femininity-masculinity: women found feminine male faces more attractive under pathogen threat, while men found feminine female faces more attractive under resource threat. This is in contrast to some previous studies, and shows that effect of ecological factors on human psychology should be submitted to a more rigorous scrutiny. The mating strategies only interacted with voice attractiveness: women rated male voices as more attractive after being primed with any type of environmental threat when considering long-term relationship context, while in men this was true when considering short-term relationship. Finally, feminine dance videos were perceived as attractive under environmental threat, irrespective of sex, type of environmental threat or mating strategy.     

Watch Out! Magnetoencephalographic Evidence for Early Modulation of Attention Orienting by Fearful Gaze Cueing

Others’ gaze and emotional facial expression are important cues for the process of attention orienting. Here, we investigated with magnetoencephalography (MEG) whether the combination of averted gaze and fearful expression may elicit a selectively early effect of attention orienting on the brain responses to targets. We used the direction of gaze of centrally presented fearful and happy faces as the spatial attention orienting cue in a Posner-like paradigm where the subjects had to detect a target checkerboard presented at gazed-at (valid trials) or non gazed-at (invalid trials) locations of the screen. We showed that the combination of averted gaze and fearful expression resulted in a very early attention orienting effect in the form of additional parietal activity between 55 and 70 ms for the valid versus invalid targets following fearful gaze cues. No such effect was obtained for the targets following happy gaze cues. This early cue-target validity effect selective of fearful gaze cues involved the left superior parietal region and the left lateral middle occipital region. These findings provide the first evidence for an effect of attention orienting induced by fearful gaze in the time range of C1. In doing so, they demonstrate the selective impact of combined gaze and fearful expression cues in the process of attention orienting.     

Face Gender Influences the Looking Preference for Smiling Expressions in 3.5-Month-Old Human Infants

Young infants are typically thought to prefer looking at smiling expressions. Although some accounts suggest that the preference is automatic and universal, we hypothesized that it is not rigid and may be influenced by other face dimensions, most notably the face’s gender. Infants are sensitive to the gender of faces; for example, 3-month-olds raised by female caregivers typically prefer female over male faces. We presented neutral versus smiling pairs of faces from the same female or male individuals to 3.5-month-old infants (n = 25), controlling for low-level cues. Infants looked longer to the smiling face when faces were female but longer to the neutral face when faces were male, i.e., there was an effect of face gender on the looking preference for smiling. The results indicate that a preference for smiling in 3.5-month-olds is limited to female faces, possibly reflective of differential experience with male and female faces.     

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.     

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.     

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.     

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.     

Reflexive social attention in monkeys and humans

For humans, social cues often guide the focus of attention. Although many nonhuman primates, like humans, live in large, complex social groups, the extent to which human and nonhuman primates share fundamental mechanisms of social attention remains unexplored. Here, we show that, when viewing a rhesus macaque looking in a particular direction, both rhesus macaques and humans reflexively and covertly orient their attention in the same direction. Specifically, when performing a peripheral visual target detection task, viewing a monkey with either its eyes alone or with both its head and eyes averted to one side facilitated the detection of peripheral targets when they randomly appeared on the same side. Moreover, viewing images of a monkey with averted gaze evoked small but systematic shifts in eye position in the direction of gaze in the image. The similar magnitude and temporal dynamics of response facilitation and eye deviation in monkeys and humans suggest shared neural circuitry mediating social attention.     

Experimental evidence that women's mate preferences are directly influenced by cues of pathogen prevalence and resource scarcity

When choosing a mate, women are thought to face a trade-off between genetic and parental quality. Recent research suggests that this trade-off is influenced by environmental factors such as pathogen prevalence and resource scarcity, which affect the relative value of genetic and parental quality to offspring fitness. To further investigate these findings, the current study primed 60 women with pathogen prevalence, resource scarcity or an irrelevant threat, before administering a forced trade-off task that assessed mate preferences for traits thought to be indicative of genetic or parental quality. Women primed with pathogen prevalence revealed greater preferences for traits indicative of genetic quality at the expense of traits indicative of parental quality. The reverse was found for women primed with resource scarcity. These findings suggest that environmental factors may directly influence women's mate preferences owing to evolved plasticity, such that mate preferences are flexible in response to environmental factors.     

Modifying the object-choice task: Is the way you look important for ravens?

Most animals seem to have difficulties in using gaze cues to find hidden food in object-choice tasks. For instance, chimpanzees usually fail in these tests, even though they are capable of following other's gaze geometrically behind barriers. Similar to chimpanzees, common ravens are skilled in tracking other's gaze but fail in object-choice tasks. We here explored whether procedural modifications, which had been used successfully in chimpanzees, would also yield positive results in ravens. In our modifications (a) the experimenter approached the cup while gazing at it, (b) the gaze cue was accompanied by a sound and (c) the experimenter could actually see the food while giving the gaze cue. Two out of seven birds performed above chance level in some of these conditions. However, we ascribe this improvement to the individuals' learning ability rather than to an understanding of the communicative nature of the task. This interpretation is further supported by results of a follow-up experiment suggesting that ravens may not rely on conspecifics' gaze cues for finding food caches in a natural foraging context. In sum, our results suggest that ravens may not transfer their gaze follow abilities to foraging situations involving hidden food.     

No Prior Entry for Threat-Related Faces: Evidence from Temporal Order Judgments

Previous research showed that threat-related faces, due to their intrinsic motivational relevance, capture attention more readily than neutral faces. Here we used a standard temporal order judgment (TOJ) task to assess whether negative (either angry or fearful) emotional faces, when competing with neutral faces for attention selection, may lead to a prior entry effect and hence be perceived as appearing first, especially when uncertainty is high regarding the order of the two onsets. We did not find evidence for this conjecture across five different experiments, despite the fact that participants were invariably influenced by asynchronies in the respective onsets of the two competing faces in the pair, and could reliably identify the emotion in the faces. Importantly, by systematically varying task demands across experiments, we could rule out confounds related to suboptimal stimulus presentation or inappropriate task demands. These findings challenge the notion of an early automatic capture of attention by (negative) emotion. Future studies are needed to investigate whether the lack of systematic bias of attention by emotion is imputed to the primacy of a non-emotional cue to resolve the TOJ task, which in turn prevents negative emotion to exert an early bottom-up influence on the guidance of spatial and temporal attention.     

Red clothing increases perceived dominance,aggression and anger

The presence and intensity of red coloration correlate with male dominance and testosterone in a variety of animal species, and even artificial red stimuli can influence dominance interactions. In humans, red stimuli are perceived as more threatening and dominant than other colours, and wearing red increases the probability of winning sporting contests. We investigated whether red clothing biases the perception of aggression and dominance outside of competitive settings, and whether red influences decoding of emotional expressions. Participants rated digitally manipulated images of men for aggression and dominance and categorized the emotional state of these stimuli. Men were rated as more aggressive and more dominant when presented in red than when presented in either blue or grey. The effect on perceived aggression was found for male and female raters, but only male raters were sensitive to red as a signal of dominance. In a categorization test, images were significantly more often categorized as ‘angry’ when presented in the red condition, demonstrating that colour stimuli affect perceptions of emotions. This suggests that the colour red may be a cue used to predict propensity for dominance and aggression in human males.