Carryover effect of joint attention to repeated events in chimpanzees and young children

Gaze following is a fundamental component of triadic social interaction which includes events and an object shared with other individuals and is found in both human and nonhuman primates. Most previous work has focused only on the immediate reaction after following another’s gaze. In contrast, this study investigated whether gaze following is retained after the observation of the other’s gaze shift, whether this retainment differs between species and age groups, and whether the retainment depends on the nature of the preceding events. In the social condition, subjects (1- and 2-year-old human children and chimpanzees) witnessed an experimenter who looked and pointed in the direction of a target lamp. In the physical condition, the target lamp blinked but the experimenter did not provide any cues. After a brief delay, we presented the same stimulus again without any cues. All subjects looked again to the target location after experiencing the social condition and thus showed a carryover effect. However, only 2-year-olds showed a carryover effect in the physical condition; 1-year-olds and chimpanzees did not. Additionally, only human children showed spontaneous interactive actions such as pointing. Our results suggest that the difference between the two age groups and chimpanzees is conceptual and not only quantitative.     

Implicit sequence learning in ring‐tailed lemurs (Lemur catta)

Implicit learning involves picking up information from the environment without explicit instruction or conscious awareness of the learning process. In nonhuman animals, conscious awareness is impossible to assess, so we define implicit learning as occurring when animals acquire information beyond what is required for successful task performance. While implicit learning has been documented in some nonhuman species, it has not been explored in prosimian primates. Here we ask whether ring‐tailed lemurs (Lemur catta) learn sequential information implicitly. We tested lemurs in a modified version of the serial reaction time task on a touch screen computer. Lemurs were required to respond to any picture within a 2 × 2 grid of pictures immediately after its surrounding border flickered. Over 20 training sessions, both the locations and the identities of the images remained constant and response times gradually decreased. Subsequently, the locations and/or the identities of the images were disrupted. Response times indicated that the lemurs had learned the physical location sequence required in original training but did not learn the identity of the images. Our results reveal that ring‐tailed lemurs can implicitly learn spatial sequences, and raise questions about which scenarios and evolutionary pressures give rise to perceptual versus motor‐implicit sequence learning.     

双通路理论视角下孤独症谱系障碍者的视线加工障碍

临床行为观察发现, 孤独症谱系障碍个体普遍存在不能与他人建立视线接触, 不能追随他人视线看向目标物体等视线加工(gaze processing)障碍。然而已有实验研究发现该群体在实验情境中普遍存在视线接触(eye contact)异常, 但其视线追随行为(gaze following)则存在正常与异常并存的现象。基于视线加工双通路理论的启示, 该障碍可能是由于视线加工皮下通路先天功能异常而皮层通路后天发展异常所致。然而, 该理论尚缺乏皮下通路先天功能异常是视线接触障碍潜在神经机制的直接证据, 还需进一步考察皮下通路先天功能异常对视线追随障碍的影响作用, 以及皮层通路后天发展异常即其补偿机制的神经回路及早期形成过程。     

Dynamic fearful gaze does not enhance attention orienting in individuals with Asperger’s disorder

Although impaired joint attention is one of the core clinical features of pervasive developmental disorder including autistic disorder and Asperger’s disorder, experimental studies failed to report its impairment. This discrepancy might be the result of differences between real-life and experimental situations. The present study examined joint attention in 11 individuals with Asperger’s disorder and 11 age-matched controls under naturalistic conditions using a target detection paradigm with dynamic emotional gaze cues. Although both groups showed gaze-triggered attention orienting as assessed by the differences in reaction time for invalid minus valid cues, enhancement of joint attention by fearful (vs. neutral) gaze was observed in the control, but not in the Asperger group. This suggests that the integration of emotion and gaze direction that elicits strong joint attention is impaired in individuals with Asperger’s disorder.     

Facial expressions modulate the ontogenetic trajectory of gaze-following among monkeys

Gaze-following, the tendency to direct one's attention to locations looked at by others, is a crucial aspect of social cognition in human and nonhuman primates. Whereas the development of gaze-following has been intensely studied in human infants, its early ontogeny in nonhuman primates has received little attention. Combining longitudinal and cross-sectional observational data from Barbary macaques at 'La Forêt des Singes', we show here that gaze-following among conspecifics develops within the first year of life with a rapid increase between 5 and 6 months, reaching adult levels at 1 year. Sex, rank, and relatedness of the animal whose gaze the subject followed did not affect gaze-following rates. Interestingly, however, the behavior was enhanced in all age classes if a gaze-cue was accompanied by a facial expression. Furthermore, the effect of facial expressions had a modulatory influence on the ontogenetic trajectory of gaze-following, suggesting that it is of functional significance in the development of the behavior. Follow-up analyses revealed that one specific facial expression that is given in response to social interactions between third parties was particularly efficient in eliciting gaze-following responses, indicating the importance of cues that are able to guide the acquisition of social information. Taken together, these results suggest that the development and the operation of gaze-following are tuned to the social and physical characteristics of a species' environment.     

Gaze following and gaze priming in lemurs

Although primates have often been found to co-orient visually with other individuals, members of these same species have usually failed to use co-orientation to find hidden food in object-choice experiments. This presents an evolutionary puzzle: what is the function of co-orientation if it is not used for a function as basic as locating resources? Co-orientation responses have not been systematically investigated in object-choice experiments, and requiring co-orientation with humans (as is typical in object-choice tasks) may underestimate other species’ abilities. Using an object-choice task with conspecific models depicted in photographs, we provide experimental evidence that two lemur species (Eulemur fulvus, n = 4, and Eulemur macaco, n = 2) co-orient with conspecifics. Secondly, by analysing together two measures that have traditionally been examined separately, we show that lemurs’ gaze following behaviour and ultimate choice are closely linked. Individuals were more likely to choose correctly after having looked in the same direction as the model, and thus chose objects correctly more often than chance. We propose a candidate system for the evolutionary origins of more complex gaze following: ‘gaze priming.’     

Audiovisual integration facilitates monkeys’ short-term memory

Many human behaviors are known to benefit from audiovisual integration, including language and communication, recognizing individuals, social decision making, and memory. Exceptionally little is known about the contributions of audiovisual integration to behavior in other primates. The current experiment investigated whether short-term memory in nonhuman primates is facilitated by the audiovisual presentation format. Three macaque monkeys that had previously learned an auditory delayed matching-to-sample (DMS) task were trained to perform a similar visual task, after which they were tested with a concurrent audiovisual DMS task with equal proportions of auditory, visual, and audiovisual trials. Parallel to outcomes in human studies, accuracy was higher and response times were faster on audiovisual trials than either unisensory trial type. Unexpectedly, two subjects exhibited superior unimodal performance on auditory trials, a finding that contrasts with previous studies, but likely reflects their training history. Our results provide the first demonstration of a bimodal memory advantage in nonhuman primates, lending further validation to their use as a model for understanding audiovisual integration and memory processing in humans.     

Geometrical gaze following in common marmosets (Callithrix jacchus)

A series of experiments investigating the degree of gaze understanding in common marmosets (Callithrix jacchus) is reported. Results show that marmosets follow the gaze of a human experimenter readily and also use the gaze to locate food in a modified version of the object choice task if influences of chance probabilities and prepotent response tendencies are controlled for. In addition, this new version of the task allows the assessment of the accuracy of gaze following. Marmosets precisely extrapolate gaze direction, past distracting objects and from considerable distances, thereby meeting the criteria of so-called geometrical gaze following. The presence of this ability in common marmosets suggests that higher forms of gaze following might be more widely distributed among nonhuman primates than previously thought.     

Dynamic fearful gaze does not enhance attention orienting in individuals with Asperger’s disorder

Although impaired joint attention is one of the core clinical features of pervasive developmental disorder including autistic disorder and Asperger’s disorder, experimental studies failed to report its impairment. This discrepancy might be the result of differences between real-life and experimental situations. The present study examined joint attention in 11 individuals with Asperger’s disorder and 11 age-matched controls under naturalistic conditions using a target detection paradigm with dynamic emotional gaze cues. Although both groups showed gaze-triggered attention orienting as assessed by the differences in reaction time for invalid minus valid cues, enhancement of joint attention by fearful (vs. neutral) gaze was observed in the control, but not in the Asperger group. This suggests that the integration of emotion and gaze direction that elicits strong joint attention is impaired in individuals with Asperger’s disorder.     

Can lemurs learn to deceive? A study in the black lemur (Eulemur macaco)

Deceptive behavior in primates has been the focus of a number of studies. Nevertheless, such abilities have never been demonstrated in prosimians. The authors' goal was to analyze possible deception in lemurs according to a paradigm used with simians. Three black lemurs were trained to communicate about the location of a hidden reward with a cooperative trainer. Afterward, when a 2nd trainer and lemurs competed to gain access to the reward, each subject differentially adapted its learned behavior to the context. Their performances with the cooperative trainer remained stable while they showed various behavioral adjustments when faced to the competitive trainer: 1 subject refused to participate, another preferentially withheld information, and the 3rd sometimes pointed deceptively to obtain the reward.     

Aping expressions? Chimpanzees produce distinct laugh types when responding to laughter of others

Humans have the ability to replicate the emotional expressions of others even when they undergo different emotions. Such distinct responses of expressions, especially positive expressions, play a central role in everyday social communication of humans and may give the responding individuals important advantages in cooperation and communication. The present work examined laughter in chimpanzees to test whether nonhuman primates also use their expressions in such distinct ways. The approach was first to examine the form and occurrence of laugh replications (laughter after the laughter of others) and spontaneous laughter of chimpanzees during social play and then to test whether their laugh replications represented laugh-elicited laugh responses (laughter triggered by the laughter of others) by using a quantitative method designed to measure responses in natural social settings. The results of this study indicated that chimpanzees produce laugh-elicited laughter that is distinct in form and occurrence from their spontaneous laughter. These findings provide the first empirical evidence that nonhuman primates have the ability to replicate the expressions of others by producing expressions that differ in their underlying emotions and social implications. The data further showed that the laugh-elicited laugh responses of the subjects were closely linked to play maintenance, suggesting that chimpanzees might gain important cooperative and communicative advantages by responding with laughter to the laughter of their social partners. Notably, some chimpanzee groups of this study responded more with laughter than others, an outcome that provides empirical support of a socialization of expressions in great apes similar to that of humans.     

Visual Attention in Real-World Conversation: Gaze Patterns Are Modulated by Communication and Group Size

Gaze behavior both initiates and maintains conversations, playing a crucial role in real-world collaboration. Hitherto, most findings on social attention stem from research using pictures of faces in the laboratory, however, attention operates differently in the real world. Thus, we know little of how gaze behavior operates in naturalistic interactions. To bridge this gap, we applied mobile eye-tracking to investigate the gaze patterns present in naturalistic conversations. Specifically, we examined gaze behavior of participants in a group of two or five, either sitting together in silence, or engaging in a conversation, in which they took turns either listening or speaking to each other. Results show that participants looked more frequently towards others when the group was communicating compared to when remaining silent, and that they looked at others more frequently when listening compared to when speaking. Furthermore, being part of a dyad led to more social attention being afforded during conversation compared to the group situation, regardless of whether subjects were listening or speaking. Meanwhile, when sitting in silence subjects showed less social gazing in a dyad than in a group of five. Our results provide qualitative and quantitative insights into the patterns of visual attention during dynamic naturalistic conversations.     

Ring-tailed lemurs (Lemur catta) exploit information about what others can see but not what they can hear

Studies suggest that haplorhine primates are sensitive to what others can see and hear. Using two experimental designs, we tested the hypothesis that ring-tailed lemurs (N = 16) are also sensitive to the visual and auditory perception of others. In the first task, we used a go/no–go design that required lemurs to exploit only auditory information. In the second task, we used a forced-choice design where lemurs competed against a human who would prevent them from obtaining food if their approaches were detected. Subjects were given the choice of obtaining food silently or noisily when the competitor’s back was turned. They were also given the choice to obtain food when the competitor could either see them or not. Here, we replicate the findings of previous studies indicating that ring-tailed lemurs are sensitive to whether they can be seen; however, we found no evidence that subjects are sensitive to whether others can hear them. Our findings suggest that ring-tailed lemurs converge with haplorhine primates only in their sensitivity to the visual information of others. The results emphasize the importance of investigating social cognition across sensory domains in order to elucidate the cognitive mechanisms that underlie apparently complex social behavior. These findings also suggest that the social dynamics of haplorhine groups impose greater cognitive demands than lemur groups, despite similarities in total group size.     

ERPs reveal similar effects of social gaze orienting and voluntary attention, and distinguish each from reflexive attention

Spatial attention can be reflexively captured by a physically salient stimulus, effortfully directed toward a relevant location, or involuntarily oriented in the direction of another person's gaze (i.e., social gaze orienting). Here, we used event-related potentials to compare the effects of these three types of orienting on multiple stages of subsequent target processing. Although gaze orienting has been associated more strongly with reflexive capture than with voluntary attention, the present data provide new evidence that the neural effects of social gaze orienting are markedly different from the effects of reflexive attentional capture by physically salient stimuli. Specifically, despite their similar behavioral effects, social gaze orienting and reflexive capture produce different effects on both early sensory processing (~120 ms; P1/N1 components) and later, higher-order processing (~300 ms; P3 component). In contrast, the effects of social gaze orienting were highly similar to those of voluntary orienting at these stages of target processing.     

读心的比较研究：非人灵长类与人类在心理理论上的异同点及其解释

利用非人灵长类开展比较研究是探索心理理论本质、起源和进化动因的重要途经。大量实证研究显示非人灵长类可以表现出一些基础心理理论成分, 包括联合注意、意图理解和一级观点采择, 这表明心理理论在灵长类动物的进化谱系中具有进化连续性。然而, 非人灵长类无法像人类一样达成二级观点采择和错误信念理解, 潜心智化假说、替代表征假说、最小限度心理理论假说和意识关系假说试图对此差异进行解释。尽管视角与具体内容不同, 但这些假说都强调, 非人灵长类无法对其他个体关于外部世界的心理信念形成表征, 信念表征是非人灵长类与人类读心能力的重要分界点。未来研究需要重点澄清共享意图、语言机制以及社会生态环境因素与心理理论产生的相互影响作用。     

Memory and attention for social threat: anxious hypercoding-avoidance and submissive gaze aversion

Rivalry for dominance is a recurrent challenge in human social interaction. During these social dominance interactions, some people rapidly break eye contact, whereas others merely try to avoid such eye-to-eye confrontations. The first is an example of submissive gaze aversion, whereas the second reflects anxious gaze avoidance. We tested these distinct forms of gaze behavior within a social-memory setting and show that anxious individuals vigilantly attend to, superiorly remember, and subsequently avoid social threats (i.e., angry faces). Furthermore, submissive individuals, as indexed by high trait anxiety and low trait anger, exhibit rapid gaze aversion from facial anger. Mechanisms of hypervigilance-avoidance thus seem to underlie natural gaze behavior and enhanced memory for threat in anxiety. Accordingly, we propose the term hypercoding-avoidance, which describes how anxious individuals habitually scan their immediate social environment for threat, remember its location, and subsequently avoid it. Moreover, this is the first experimental evidence showing that submissive gaze aversion is distinct from anxious gaze avoidance.     

Mechanisms Linking Early Experience and the Emergence of Emotions: Illustrations From the Study of Maltreated Children

Emotions are complex processes that are essential for survival and adaptation. Recent studies of children and animals are shedding light on how the developing brain learns to rapidly respond to signals in the environment, assess the emotional significance of this information, and in so doing adaptively regulate subsequent behavior. Here, I describe studies of children and nonhuman primates who are developing within emotionally aberrant environments. Examining these populations provides new insights on the ways in which social or interpersonal contexts influence development of the neural systems underlying emotional behavior.     

Attention orienting by eye gaze and arrows reveals flexibility to environmental changes

This study aimed to evaluate the difference in non-predictive cues between gaze and arrows in attention orienting. Attention orienting was investigated with gaze or arrows as separate cues in a simple condition (i.e., block design) in Experiment 1 and in an unpredictable condition (i.e., randomized design) in Experiment 2. Two kinds of sound (voice and tone) stimuli were used as targets. Results showed that gaze and arrow cues induced enhanced attention orienting to a voice versus tone target in the block condition. However, in the randomized condition, enhanced attention orienting to a voice versus tone target was found in gaze but not arrow cues. The congruency of the meaning between a social cue (i.e., gaze) and a social target (i.e., voice) was clear in the randomized but not blocked design, because social gaze and non-social arrow cues were implemented in the same block. Thus, attention orienting might be mediated by the associated relationship of cue–target in a randomized condition, as an enhanced orienting effect was found when the associated relationship of cue–target was strong (i.e., social cue and target). The present study suggests that the difference in attention orienting between gaze and arrows is apparent in a randomized design (the unpredictable condition), and people employ a flexibly strategy of orienting to better respond to environmental changes.     

The effect of gaze on gaze direction while looking at art

In highly controlled cuing experiments, conspecific gaze direction has powerful effects on an observer’s attention. We explored the generality of this effect by using paintings in which the gaze direction of a key character had been carefully manipulated. Our observers looked at these paintings in one of three instructional states (neutral, social, or spatial) while we monitored their eye movements. Overt orienting was much less influenced by the critical gaze direction than what the cuing literature might suggest: An analysis of the direction of saccades following the first fixation of the critical gaze showed that observers were weakly biased to orient in the direction of the gaze. Over longer periods of viewing, however, this effect disappeared for all but the social condition. This restriction of gaze as an attentional cue to a social context is consistent with the idea that the evolution of gaze direction detection is rooted in social communication. The picture stimuli from this experiment can be downloaded from the Psychonomic Society’s Archive of Norms, Stimuli, and Data, www.psychonomic.org/archive.     

Orienting and maintenance of gaze to facial expressions in social anxiety

In 2 experiments, the authors tested predictions from cognitive models of social anxiety regarding attentional biases for social and nonsocial cues by monitoring eye movements to pictures of faces and objects in high social anxiety (HSA) and low social anxiety (LSA) individuals. Under no-stress conditions (Experiment 1), HSA individuals initially directed their gaze toward neutral faces, relative to objects, more often than did LSA participants. However, under social-evaluative stress (Experiment 2), HSA individuals showed reduced biases in initial orienting and maintenance of gaze on faces (cf. objects) compared with the LSA group. HSA individuals were also relatively quicker to look at emotional faces than neutral faces but looked at emotional faces for less time, compared with LSA individuals, consistent with a vigilant-avoidant pattern of bias.