Gaze following in human infants depends on communicative signals

Humans are extremely sensitive to ostensive signals, like eye contact or having their name called, that indicate someone's communicative intention toward them [1-3]. Infants also pay attention to these signals [4-6], but it is unknown whether they appreciate their significance in the initiation of communicative acts. In two experiments, we employed video presentation of an actor turning toward one of two objects and recorded infants' gaze-following behavior [7-13] with eye-tracking techniques [11, 12]. We found that 6-month-old infants followed the adult's gaze (a potential communicative-referential signal) toward an object only when such an act is preceded by ostensive cues such as direct gaze (experiment 1) and infant-directed speech (experiment 2). Such a link between the presence of ostensive signals and gaze following suggests that this behavior serves a functional role in assisting infants to effectively respond to referential communication directed to them. Whereas gaze following in many nonhuman species supports social information gathering [14-18], in humans it initially appears to reflect the expectation of a more active, communicative role from the information source.     

Dogs' gaze following is tuned to human communicative signals

Recent evidence suggests that preverbal infants' gaze following can be triggered only if an actor's head turn is preceded by the expression of communicative intent [1]. Such connectedness between ostensive and referential signals may be uniquely human, enabling infants to effectively respond to referential communication directed to them. In the light of increasing evidence of dogs' social communicative skills [2], an intriguing question is whether dogs' responsiveness to human directional gestures [3] is associated with the situational context in an infant-like manner. Borrowing a method used in infant studies [1], dogs watched video presentations of a human actor turning toward one of two objects, and their eye-gaze patterns were recorded with an eye tracker. Results show a higher tendency of gaze following in dogs when the human's head turning was preceded by the expression of communicative intent (direct gaze, addressing). This is the first evidence to show that (1) eye-tracking techniques can be used for studying dogs' social skills and (2) the exploitation of human gaze cues depends on the communicatively relevant pattern of ostensive and referential signals in dogs. Our findings give further support to the existence of a functionally infant-analog social competence in this species.     

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.     

Early cortical specialization for face-to-face communication in human infants

This study examined the brain bases of early human social cognitive abilities. Specifically, we investigated whether cortical regions implicated in adults' perception of facial communication signals are functionally active in early human development. Four-month-old infants watched two kinds of dynamic scenarios in which a face either established mutual gaze or averted its gaze, both of which were followed by an eyebrow raise with accompanying smile. Haemodynamic responses were measured by near-infrared spectroscopy, permitting spatial localization of brain activation (experiment 1), and gamma-band oscillatory brain activity was analysed from electroencephalography to provide temporal information about the underlying cortical processes (experiment 2). The results revealed that perceiving facial communication signals activates areas in the infant temporal and prefrontal cortex that correspond to the brain regions implicated in these processes in adults. In addition, mutual gaze itself, and the eyebrow raise with accompanying smile in the context of mutual gaze, produce similar cortical activations. This pattern of results suggests an early specialization of the cortical network involved in the perception of facial communication cues, which is essential for infants' interactions with, and learning from, others.     

Predicting Aggressive Tendencies by Visual Attention Bias Associated with Hostile Emotions

The goal of the current study is to clarify the relationship between social information processing (e.g., visual attention to cues of hostility, hostility attribution bias, and facial expression emotion labeling) and aggressive tendencies. Thirty adults were recruited in the eye-tracking study that measured various components in social information processing. Baseline aggressive tendencies were measured using the Buss-Perry Aggression Questionnaire (AQ). Visual attention towards hostile objects was measured as the proportion of eye gaze fixation duration on cues of hostility. Hostility attribution bias was measured with the rating results for emotions of characters in the images. The results show that the eye gaze duration on hostile characters was significantly inversely correlated with the AQ score and less eye contact with an angry face. The eye gaze duration on hostile object was not significantly associated with hostility attribution bias, although hostility attribution bias was significantly positively associated with the AQ score. Our findings suggest that eye gaze fixation time towards non-hostile cues may predict aggressive tendencies.     

Infant neural sensitivity to dynamic eye gaze is associated with later emerging autism

Autism spectrum disorders (henceforth autism) are diagnosed in around 1% of the population [1]. Familial liability confers risk for a broad spectrum of difficulties including the broader autism phenotype (BAP) [2, 3]. There are currently no reliable predictors of autism in infancy, but characteristic behaviors emerge during the second year, enabling diagnosis after this age [4, 5]. Because indicators of brain functioning may be sensitive predictors, and atypical eye contact is characteristic of the syndrome [6-9] and the BAP [10, 11], we examined whether neural sensitivity to eye gaze during infancy is associated with later autism outcomes [12, 13]. We undertook a prospective longitudinal study of infants with and without familial risk for autism. At 6-10 months, we recorded infants' event-related potentials (ERPs) in response to viewing faces with eye gaze directed toward versus away from the infant [14]. Longitudinal analyses showed that characteristics of ERP components evoked in response to dynamic eye gaze shifts during infancy were associated with autism diagnosed at 36 months. ERP responses to eye gaze may help characterize developmental processes that lead to later emerging autism. Findings also elucidate the mechanisms driving the development of the social brain in infancy.     

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.     

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.     

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.     

Attachment and social preferences in cooperatively-reared cotton-top tamarins

In many primate species a close attachment between mother and infant provides a secure base for the infant when the infant is frightened or under stress. In cooperatively breeding primates infant carrying is divided among several individuals in the group, with the mother often doing little more than nursing. In these species it is not clear which individual would best serve as a secure base for the infant. We studied eight infant cotton-top tamarins from birth through 20 weeks of age, noting who carried the infant during the first 100 days, who transferred food with the infants, and, as infants became independent, with whom they associated during social play and affiliative behavior. From week 9 to week 20, when infants were independent of carriers most of the time, we presented families with six trials (once every 2 weeks) with a threatening stimulus (a human dressed in a lab coat and wearing an animal mask). Infants played primarily with their twin or youngest sibling and had affiliative interactions with many family members. However, in fearful situations, infants ran to those who had carried them and transferred food with them the most-their father or oldest brother (never to the mother). Although adults increased rates of mobbing calls in response to the threat, infants significantly reduced their vocalization rate. For these cooperatively breeding monkeys, the attachment object for infants is the family member that invested the most effort in carrying the infant and transferring food with the infant. These results parallel and extend results from bi-parental infant care species in which the father serves as the primary attachment figure.     

Diagnostic features of emotional expressions are processed preferentially

Diagnostic features of emotional expressions are differentially distributed across the face. The current study examined whether these diagnostic features are preferentially attended to even when they are irrelevant for the task at hand or when faces appear at different locations in the visual field. To this aim, fearful, happy and neutral faces were presented to healthy individuals in two experiments while measuring eye movements. In Experiment 1, participants had to accomplish an emotion classification, a gender discrimination or a passive viewing task. To differentiate fast, potentially reflexive, eye movements from a more elaborate scanning of faces, stimuli were either presented for 150 or 2000 ms. In Experiment 2, similar faces were presented at different spatial positions to rule out the possibility that eye movements only reflect a general bias for certain visual field locations. In both experiments, participants fixated the eye region much longer than any other region in the face. Furthermore, the eye region was attended to more pronouncedly when fearful or neutral faces were shown whereas more attention was directed toward the mouth of happy facial expressions. Since these results were similar across the other experimental manipulations, they indicate that diagnostic features of emotional expressions are preferentially processed irrespective of task demands and spatial locations. Saliency analyses revealed that a computational model of bottom-up visual attention could not explain these results. Furthermore, as these gaze preferences were evident very early after stimulus onset and occurred even when saccades did not allow for extracting further information from these stimuli, they may reflect a preattentive mechanism that automatically detects relevant facial features in the visual field and facilitates the orientation of attention towards them. This mechanism might crucially depend on amygdala functioning and it is potentially impaired in a number of clinical conditions such as autism or social anxiety disorders.     

Shyness in Early Infancy: Approach-Avoidance Conflicts in Temperament and Hypersensitivity to Eyes during Initial Gazes to Faces

‘Infant shyness’, in which infants react shyly to adult strangers, presents during the third quarter of the first year. Researchers claim that shy children over the age of three years are experiencing approach-avoidance conflicts. Counter-intuitively, shy children do not avoid the eyes when scanning faces; rather, they spend more time looking at the eye region than non-shy children do. It is currently unknown whether young infants show this conflicted shyness and its corresponding characteristic pattern of face scanning. Here, using infant behavioral questionnaires and an eye-tracking system, we found that highly shy infants had high scores for both approach and fear temperaments (i.e., approach-avoidance conflict) and that they showed longer dwell times in the eye regions than less shy infants during their initial fixations to facial stimuli. This initial hypersensitivity to the eyes was independent of whether the viewed faces were of their mothers or strangers. Moreover, highly shy infants preferred strangers with an averted gaze and face to strangers with a directed gaze and face. This initial scanning of the eye region and the overall preference for averted gaze faces were not explained solely by the infants’ age or temperament (i.e., approach or fear). We suggest that infant shyness involves a conflict in temperament between the desire to approach and the fear of strangers, and this conflict is the psychological mechanism underlying infants’ characteristic behavior in face scanning.     

Individual Differences in Personality Predict How People Look at Faces

Background

Determining the ways in which personality traits interact with contextual determinants to shape social behavior remains an important area of empirical investigation. The specific personality trait of neuroticism has been related to characteristic negative emotionality and associated with heightened attention to negative, emotionally arousing environmental signals. However, the mechanisms by which this personality trait may shape social behavior remain largely unspecified.

Methodology/Principal Findings

We employed eye tracking to investigate the relationship between characteristics of visual scanpaths in response to emotional facial expressions and individual differences in personality. We discovered that the amount of time spent looking at the eyes of fearful faces was positively related to neuroticism.

Conclusions/Significance

This finding is discussed in relation to previous behavioral research relating personality to selective attention for trait-congruent emotional information, neuroimaging studies relating differences in personality to amygdala reactivity to socially relevant stimuli, and genetic studies suggesting linkages between the serotonin transporter gene and neuroticism. We conclude that personality may be related to interpersonal interaction by shaping aspects of social cognition as basic as eye contact. In this way, eye gaze represents a possible behavioral link in a complex relationship between genes, brain function, and personality.     

Dogs Evaluate Threatening Facial Expressions by Their Biological Validity – Evidence from Gazing Patterns

Appropriate response to companions’ emotional signals is important for all social creatures. The emotional expressions of humans and non-human animals have analogies in their form and function, suggesting shared evolutionary roots, but very little is known about how animals other than primates view and process facial expressions. In primates, threat-related facial expressions evoke exceptional viewing patterns compared with neutral or positive stimuli. Here, we explore if domestic dogs (Canis familiaris) have such an attentional bias toward threatening social stimuli and whether observed emotional expressions affect dogs’ gaze fixation distribution among the facial features (eyes, midface and mouth). We recorded the voluntary eye gaze of 31 domestic dogs during viewing of facial photographs of humans and dogs with three emotional expressions (threatening, pleasant and neutral). We found that dogs’ gaze fixations spread systematically among facial features. The distribution of fixations was altered by the seen expression, but eyes were the most probable targets of the first fixations and gathered longer looking durations than mouth regardless of the viewed expression. The examination of the inner facial features as a whole revealed more pronounced scanning differences among expressions. This suggests that dogs do not base their perception of facial expressions on the viewing of single structures, but the interpretation of the composition formed by eyes, midface and mouth. Dogs evaluated social threat rapidly and this evaluation led to attentional bias, which was dependent on the depicted species: threatening conspecifics’ faces evoked heightened attention but threatening human faces instead an avoidance response. We propose that threatening signals carrying differential biological validity are processed via distinctive neurocognitive pathways. Both of these mechanisms may have an adaptive significance for domestic dogs. The findings provide a novel perspective on understanding the processing of emotional expressions and sensitivity to social threat in non-primates.     

In the eye of the beholder: reduced threat-bias and increased gaze-imitation towards reward in relation to trait anger

The gaze of a fearful face silently signals a potential threat's location, while the happy-gaze communicates the location of impending reward. Imitating such gaze-shifts is an automatic form of social interaction that promotes survival of individual and group. Evidence from gaze-cueing studies suggests that covert allocation of attention to another individual's gaze-direction is facilitated when threat is communicated and further enhanced by trait anxiety. We used novel eye-tracking techniques to assess whether dynamic fearful and happy facial expressions actually facilitate automatic gaze-imitation. We show that this actual gaze-imitation effect is stronger when threat is signaled, but not further enhanced by trait anxiety. Instead, trait anger predicts facilitated gaze-imitation to reward, and to reward compared to threat. These results agree with an increasing body of evidence on trait anger sensitivity to reward.     

Selective prefrontal cortex responses to joint attention in early infancy

The process by which two people share attention towards the same object or event is called joint attention. Joint attention and the underlying triadic representations between self, other person and object are thought to be unique to humans, supporting teaching, cooperation and language learning. Despite the progress that has been made in understanding the behavioural importance of joint attention during early social development, almost nothing is known about the brain substrate that supports joint attention in the developing infant. We examined responses in five-month-old infants'' prefrontal cortex during triadic social interactions using near-infrared spectroscopy. The results demonstrate that, even by the age of five months, infants are sensitive to triadic interactions and, like adults, they recruit a specific brain region localized in left dorsal prefrontal cortex when engaged in joint attention with another person. This suggests that the human infant is neurobiologically prepared for sharing attention with other humans, which may provide the basis for a wide variety of uniquely human social and cultural learning processes.     

The range of action of the mother and the avoidance of big novel objects in long-tailed macaques

Most surrogate-reared long-tailed macaques persistently avoid a big novel object, whereas most mother-reared subjects approach it. A striking difference between these attachment figures is that the mothers moved about with their infants, whereas the surrogates were fixed to the wall In this experiment, we aimed to find out whether mobility of the attachment figure plays a part in the development of an infant’s responses to big novel objects. We studied the effects of mobility of the attachment figure by restraining mothers in their range of action. We confined mothers of the experimental group in a small part of the home cage. Their infants could leave the cage in which their mothers were restrained. Infants that were growing up with unrestrained mothers made up the control group. At two different ages all infants encountered a big novel object. We used two different objects. We found that the range of action of the mother did not significantly affect the responses of infants to big novel objects. As in the previous studies, most of the mother-reared monkeys approached the objects. The age at which an infant was first exposed to an object did not significantly affect its behavior toward it. Further, the two different objects evoked the same reactions.     

Social cognition

Social cognition concerns the various psychological processes that enable individuals to take advantage of being part of a social group. Of major importance to social cognition are the various social signals that enable us to learn about the world. Such signals include facial expressions, such as fear and disgust, which warn us of danger, and eye gaze direction, which indicate where interesting things can be found. Such signals are particularly important in infant development. Social referencing, for example, refers to the phenomenon in which infants refer to their mothers' facial expressions to determine whether or not to approach a novel object. We can learn a great deal simply by observing others. Much of this signalling seems to happen automatically and unconsciously on the part of both the sender and the receiver. We can learn to fear a stimulus by observing the response of another, in the absence of awareness of that stimulus. By contrast, learning by instruction, rather than observation, does seem to depend upon awareness of the stimulus, since such learning does not generalize to situations where the stimulus is presented subliminally. Learning by instruction depends upon a meta-cognitive process through which both the sender and the receiver recognize that signals are intended to be signals. An example would be the 'ostensive' signals that indicate that what follows are intentional communications. Infants learn more from signals that they recognize to be instructive. I speculate that it is this ability to recognize and learn from instructions rather than mere observation which permitted that advanced ability to benefit from cultural learning that seems to be unique to the human race.     

Active gaze control improves optic flow-based segmentation and steering

An observer traversing an environment actively relocates gaze to fixate objects. Evidence suggests that gaze is frequently directed toward the center of an object considered as target but more likely toward the edges of an object that appears as an obstacle. We suggest that this difference in gaze might be motivated by specific patterns of optic flow that are generated by either fixating the center or edge of an object. To support our suggestion we derive an analytical model that shows: Tangentially fixating the outer surface of an obstacle leads to strong flow discontinuities that can be used for flow-based segmentation. Fixation of the target center while gaze and heading are locked without head-, body-, or eye-rotations gives rise to a symmetric expansion flow with its center at the point being approached, which facilitates steering toward a target. We conclude that gaze control incorporates ecological constraints to improve the robustness of steering and collision avoidance by actively generating flows appropriate to solve the task.