Social monitoring in a primate group: the relationship between visual attention and hierarchical ranks

McNelis, Nicole L.; Boatright‐Horowitz, Su L.

doi:10.1007/s100710050008

Cited by 71 publications

(65 citation statements)

References 13 publications

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“…Specifically, our results are consistent with a model in which OT alleviates a species-typical state of vigilance toward social threats. For most primates, dominant individuals are potential sources of threat and are preferentially attended over other social cues (18,22). Similarly, primates are more vigilant for unfamiliar animals relative to familiar individuals (23).…”

Section: Discussionmentioning

confidence: 99%

Oxytocin blunts social vigilance in the rhesus macaque

Ebitz

Watson

2013

Proc. Natl. Acad. Sci. U.S.A.

124

151

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Exogenous application of the neuromodulatory hormone oxytocin (OT) promotes prosocial behavior and can improve social function. It is unclear, however, whether OT promotes prosocial behavior per se, or whether it facilitates social interaction by reducing a state of vigilance toward potential social threats. To disambiguate these two possibilities, we exogenously delivered OT to male rhesus macaques, which have a characteristic pattern of species-typical social vigilance, and examined their performance in three social attention tasks. We first determined that, in the absence of competing task demands or goals, OT increased attention to faces and eyes, as in humans. By contrast, OT reduced species typical social vigilance for unfamiliar, dominant, and emotional faces in two additional tasks. OT eliminated the emergence of a typical state of vigilance when dominant face images were available during a social image choice task. Moreover, OT improved performance on a reward-guided saccade task, despite salient social distractors: OT reduced the interference of unfamiliar faces, particularly emotional ones, when these faces were task irrelevant. Together, these results demonstrate that OT suppresses vigilance toward potential social threats in the rhesus macaque. We hypothesize that a basic role for OT in regulating social vigilance may have facilitated the evolution of prosocial behaviors in humans.attention | primates | face gaze | neuropeptide

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Section: Discussionmentioning

confidence: 99%

Oxytocin blunts social vigilance in the rhesus macaque

Ebitz

Watson

2013

Proc. Natl. Acad. Sci. U.S.A.

124

151

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“…For instance, even shortly after birth, human infants look longer at faces than at similar nonface stimuli (49). Likewise, nonhuman primates spend more time looking at pictures of faces directed toward them compared with pictures of faces with averted gaze (50), and direct their gaze more often toward higher-ranking than lower-ranking animals (51). Furthermore, active social interactions such as cooperative transactions (52,53) or the opportunity to punish a traitor (54), which can be understood using a game theoretic framework (55), can be as motivating as primary rewards in humans.…”

Section: Parallels Between Social and Nonsocial Behaviorsmentioning

confidence: 99%

Neuroethology of primate social behavior

Chang¹,

Brent²,

Adams³

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

136

107

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A neuroethological approach to human and nonhuman primate behavior and cognition predicts biological specializations for social life. Evidence reviewed here indicates that ancestral mechanisms are often duplicated, repurposed, and differentially regulated to support social behavior. Focusing on recent research from nonhuman primates, we describe how the primate brain might implement social functions by coopting and extending preexisting mechanisms that previously supported nonsocial functions. This approach reveals that highly specialized mechanisms have evolved to decipher the immediate social context, and parallel circuits have evolved to translate social perceptual signals and nonsocial perceptual signals into partially integrated social and nonsocial motivational signals, which together inform general-purpose mechanisms that command behavior. Differences in social behavior between species, as well as between individuals within a species, result in part from neuromodulatory regulation of these neural circuits, which itself appears to be under partial genetic control. Ultimately, intraspecific variation in social behavior has differential fitness consequences, providing fundamental building blocks of natural selection. Our review suggests that the neuroethological approach to primate behavior may provide unique insights into human psychopathology.decision | evolution | reward | serotonin | oxytocin S ensitivity and responsiveness to information about others is critical for human health (1, 2), survival (3), and even financial success (4). To navigate our social worlds, we track the behavior of others and form models of their intentions and emotional states, we actively seek out and exchange information about others, and we flexibly alter our behavior in response to what we know about others. These faculties are so important to human behavior that their disruption constitutes psychopathology (5, 6). These specializations for social behavior reflect a rich evolutionary heritage of adaptation to group life (7-9). Like humans, many nonhuman primates also live in large groups characterized by patterns of social behaviors like grooming, imitative and cooperative foraging, differentiated affiliative relationships, ritualized courtship and mating behavior, and competitive interactions structured by social dominance (10, 11). Not surprisingly, the ability to deftly navigate the social environment has observable consequences for reproductive success in some nonhuman primates (12). Evolutionary Perspective on Social BehaviorSocial behavior places strong and unique demands on the nervous system. Across primate species, group size (a potential proxy of social complexity) is correlated with forebrain volume, after correcting for body size (9). Additional brain tissue beyond that required to maintain a body of a particular size is costly, in both developmental complexity and metabolic demands (7, 13-15). Indeed, social complexity and the elaboration of neural mechanisms to support it are associated with diets high in dependa...

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“…Ring-tailed lemurs also show spontaneous gaze following of other social group members in their natural environment, suggesting that social attention evolved early in species that interact in social groups (Shepherd & Platt, 2008). Chance (1967) hypothesized that social attention would reflect the dominance hierarchy of primate groups, such that the dominant individual receives the greatest number of glances, and a recent study of patas monkeys supported this prediction (McNelis & Boatright-Horowitz, 1998). It has also been demonstrated that the effectiveness of gaze as a social cue depends on the relative social status of the individual: low status monkeys reflexively follow the gaze of any familiar monkey, but high-status macaques will only respond in this way to other high-status animals (Shepherd, Deaner, & Platt, 2006).…”

Section: Introductionmentioning

confidence: 99%

Gaze allocation in a dynamic situation: Effects of social status and speaking

et al. 2010

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a b s t r a c tHuman visual attention operates in a context that is complex, social and dynamic. To explore this, we recorded people taking part in a group decision-making task and then showed video clips of these situations to new participants while tracking their eye movements. Observers spent the majority of time looking at the people in the videos, and in particular at their eyes and faces. The social status of the people in the clips had been rated by their peers in the group task, and this status hierarchy strongly predicted where eyetracker participants looked: high-status individuals were gazed at much more often, and for longer, than low-status individuals, even over short, 20-s videos. Fixation was temporally coupled to the person who was talking at any one time, but this did not account for the effect of social status on attention. These results are consistent with a gaze system that is attuned to the presence of other individuals, to their social status within a group, and to the information most useful for social interaction.

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Social monitoring in a primate group: the relationship between visual attention and hierarchical ranks

Cited by 71 publications

References 13 publications

Oxytocin blunts social vigilance in the rhesus macaque

Oxytocin blunts social vigilance in the rhesus macaque

Neuroethology of primate social behavior

Gaze allocation in a dynamic situation: Effects of social status and speaking

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