Reflexive social attention in monkeys and humans (original) (raw)
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Social Interactions through the Eyes of Macaques and Humans
PLoS ONE, 2013
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.
Social status gates social attention in monkeys.
2006
Humans rapidly shift attention in the direction other individuals are looking, following gaze in a manner suggestive of an obligatory social reflex [1–4]. Monkeys' attention also follows gaze, and the similar magnitude and time-course of gazefollowing in rhesus macaques and humans [5] is indicative of shared neural mechanisms. Here we show that low-status male rhesus macaques reflexively follow the gaze of all familiar rhesus macaques, but high-status macaques selectively follow the gaze only of other high-status monkeys.
Reflexive gaze following in common marmoset monkeys
2019
ABSTRACTThe ability to extract the direction of the other’s gaze allows us to shift our attention to an object of interest to the other and to establish joint attention. By mapping one’s own expectations, desires and intentions on the object of joint attention, humans develop a Theory of (the other’s) Mind (TOM), a functional sequence possibly disrupted in autism. Although old world monkeys probably do not possess a TOM, they follow the other’s gaze and they establish joint attention. Gaze following of both humans and old world monkeys fulfills Fodor’s criteria of a domain specific function and is orchestrated by very similar cortical architectures, strongly suggesting homology. Also new world monkeys, a primate suborder that split from the old world monkey line about 35 million years ago, have complex social structures. One member of this group, the common marmoset (Callithrix jacchus), has received increasing interest as a potential model in studies of normal and disturbed human s...
To move or not to move: How apes adjust to the attentional state of others
Interaction Studies, 2004
A previous observational study suggested that when faced with a partner with its back turned, chimpanzees tend to move around to the front of a non-attending partner and then gesture -rather than gesturing once to attract attention and then again to convey a specific intent. We investigated this preference experimentally by presenting six orangutans, five gorillas, nine chimpanzees, and four bonobos with a food begging situation in which we varied the body orientation of an experimenter (E) with respect to the subject (front vs. back) and the location of the food (in front or behind E). These manipulations allowed us to measure whether subjects preferred to move around to face E or to use signals to attract her attention before they begged for food. Results showed that all species moved around to face E and then produced visual gestures, instead of using tactile/ auditory gestures behind E to call her attention. Species differences were apparent particularly when the food and E were in different locations. Unlike gorillas and orangutans, chimpanzees and bonobos (from genus Pan) produced their gestures in front of E in all conditions, including that in which subjects had to leave the food behind to communicate with her. Implications of these results are discussed in the context of the evolution of social cognition in great apes.
Frontiers in Psychology, 2012
Primates live in complex social groups and rely on social cues to direct their attention. For example, primates react faster to an unpredictable stimulus after seeing a conspecific looking in the direction of that stimulus. In the current study we tested the specificity of facial cues (gaze direction) for orienting attention and their interaction with other cues that are known to guide attention. In particular, we tested whether macaque monkeys only respond to gaze cues from conspecifics or if the effect generalizes across species. We found an attentional advantage of conspecific faces over human and cartoon faces. Because gaze cues are often conveyed by gesture, we also explored the effect of image motion (a simulated glance) on the orienting of attention in monkeys. We found that the simulated glance did not significantly enhance the speed of orienting for monkey-face stimuli, but had a significant effect for images of human faces. Finally, because gaze cues presumably guide attention toward relevant or rewarding stimuli, we explored whether orienting of attention was modulated by reward predictiveness. When the cue predicted reward location, face, and non-face cues were effective in speeding responses toward the cued location. This effect was strongest for conspecific faces. In sum, our results suggest that while conspecific gaze cues activate an intrinsic process that reflexively directs spatial attention, its effect is relatively small in comparison to other features including motion and reward predictiveness. It is possible that gaze cues are more important for decision-making and voluntary orienting than for reflexive orienting.
Animal cognition, 2015
The present study tested intentionality of a learned begging gesture and attention-reading abilities in rhesus macaques (Macaca mulatta). Subjects were trained to produce a begging gesture towards a hidden food reward that could be delivered by a human experimenter. More specifically, we investigated which attentional cues-body, face and/or eyes orientation of a human partner-were taken into account by the macaques in order to communicate with her. Our results provide strong evidence of intentional communication: the monkeys adjusted their behaviour to that of the partner. The latter's attentional state influenced the monkeys' likelihood of performing begging gestures and showing gaze alternation between the partner and the hidden food. By contrast, we found no evidence of attention-getting behaviours, persistence or elaboration of new communicative behaviours. Our results also showed that rhesus macaques discriminated gross cues including the presence, body and face orienta...
Live Interaction Distinctively Shapes Social Gaze Dynamics in Rhesus Macaques
Journal of Neurophysiology, 2016
The dynamic interaction of gaze between individuals is a hallmark of social cognition. However, very few studies have examined social gaze dynamics after mutual eye contact during real-time interactions. We used a highly quantifiable paradigm to assess social gaze dynamics between pairs of monkeys and modeled these dynamics using an exponential decay function to investigate sustained attention after mutual eye contact. When monkeys were interacting with real partners compared with static images and movies of the same monkeys, we found a significant increase in the proportion of fixations to the eyes and a smaller dispersion of fixations around the eyes, indicating enhanced focal attention to the eye region. Notably, dominance and familiarity between the interacting pairs induced separable components of gaze dynamics that were unique to live interactions. Gaze dynamics of dominant monkeys after mutual eye contact were associated with a greater number of fixations to the eyes, whereas...
An analysis of gaze following to a hidden location in long-tailed macaques (Macaca fascicularis)
Behaviour, 2012
Gaze following, the ability to track the direction of another's gaze, is thought to be an important component of human and animal social cognition. Several animal species attend to the gaze direction of others, but in Old World monkeys it remains unclear whether this behaviour is based on a simple co-orientation mechanism or on a more sophisticated perception of the other's visual behaviour. The capacity to follow another's gaze to a location hidden behind a physical obstacle has been argued to indicate refined skills in determining the exact direction of the other's gaze ('geometrical gaze following') and a representation of space outside one's own visual field. Human infants, great apes, new world monkeys, wolves (Canis lupus) and ravens (Corvus corax) have been shown to have this capacity. We investigated whether long-tailed macaques (Macaca fascicularis), an Old World monkey, follow conspecific gaze, indicated by head direction and visual orientation, to a hidden location. When a conspecific demonstrator gazed at a mirror hidden behind a barrier, subjects relocated to a position where they could see the mirror location and showed a trend, not statistically significant, to direct more focussed looks behind the barrier than in a situation where there was no conspicuous gaze cue by the demonstrator. The strength of this reaction was greatest in those individuals that looked most frequently at the demonstrator. Thus, long-tailed macaques may follow gaze to a hidden location, suggesting that they possess geometrical gaze following and represent space outside their own visual field. In addition, this capacity may be widespread across the animal kingdom.
Focus on the essential: all great apes know when others are being attentive
Animal Cognition, 2011
When begging for food, all great ape species are sensitive to a human's attention. However, studies investigating which cues are relevant for chimpanzees to assess the attentional state of others have produced highly inconsistent results. Some have suggested chimpanzees differentiate attention based on the status of the face or even the eyes, while others have indicated that body posture alone is the relevant cue. Kaminski et al. (Anim Cogn 7:216-223, 2004) compared the behaviour of chimpanzees, bonobos and orangutans while begging for food from a human experimenter who systematically varied his face and body orientation. Their results indicated that both factors, face and body orientation, affect apes' begging behaviour. The authors claimed that while body orientation provides information about the experimenter's general disposition to offer food, the visibility of the face provides information about the human's attentional state. In the current study, we tested this hypothesis with all four great apes species. However, unlike Kaminski et al. (Anim Cogn 7:216-223, 2004), the experimenter was able to hand over food regardless of body orientation. The results show that as soon as the offering of the food was no longer restricted, the orientation of the face became the key factor. Therefore, we present the first evidence that all great ape species are able to assess the attentional state of a recipient based on the orientation of the face.