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Differences in how macaques monitor others: Does serotonin play a central role?

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Primates must balance the need to monitor other conspecifics to gain social information while not losing other resource opportunities. We consolidate evidence across the fields of primatology, psychology, and neuroscience to examine individual, population, and species differences in how primates, particularly macaques, monitor conspecifics. We particularly consider the role of serotonin in mediating social competency via social attention, aggression, and dominance behaviors. Finally, we consider how the evolution of variation in social tolerance, aggression, and social monitoring might be explained by differences in serotonergic function in macaques. This article is categorized under: Economics > Interactive Decision‐Making Psychology > Comparative Psychology Neuroscience > Behavior Cognitive Biology > Evolutionary Roots of Cognition
Monitoring others for gaining social information in primates. (a) Many primate species gather social information by either monitoring others when information is directed from a conspecific “A” to themselves (direct‐social monitoring) or when information is communicated between conspecific “A” to conspecific “‘B” (indirect‐social, or third‐party, monitoring). (b) Rhesus macaques detect faces as early as 3 weeks of age, and this detection becomes biased towards conspecific faces by 3 months. When 3‐week‐old macaques were presented with an image of a macaque, chimpanzee, or otter face in an array with 9 non‐face objects they looked at faces (colored bars connected with black dashed lines) longer than non‐face objects (gray bars connected with gray dashed lines). By 3 months, they also looked at macaque faces significantly longer than chimpanzee faces and otter faces. *p < 0.05. **p < 0.016. Reproduced and adapted with permission from Simpson et al. (). (c) When humans and rhesus macaques view natural scene videos featuring rhesus macaques, humans, or cartoon characters, gaze fixation locations are not predicted by a model that only considers low‐level visual characteristics (e.g., contrast, stimulus orientation). Instead, the viewed locations often feature social agents and the targets of agents' actions and attention. Reproduced and adapted with permission from Shepherd, Steckenfinger, Hasson, and Ghazanfar (). (d) Rhesus macaques are willing to forgo juice rewards in order to view female perinea and high‐ranking male faces, but require extra juice rewards in order to choose to view low‐ranking male faces and non‐social stimuli. Reproduced and adapted with permission from Deaner, Khera, and Platt ()
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Diversity in social tolerance in macaque species is related to diversity in serotonergic function, and potentially impacts diversity in dominance rank, aggression, and social monitoring. (a) Left panel: Central concentrations of the serotonin metabolite (5‐HIAA) are inversely correlated with escalated aggression scores, or the proportion of all aggressive acts that were characterized by high‐intensity aggression, in rhesus macaques and pigtailed macaques. The inset shows that rhesus macaques have lower average CSF‐5‐HIAA than pigtailed macaques. Reproduced and adapted with permission from Westergaard et al. (). Middle panel: High‐ranking female macaques exhibit relatively higher central concentrations of 5‐HIAA than low‐ranking females. Reproduced and adapted with permission from Higley, King, Hasert, et al. (). Right panel: Animals with relatively lower concentrations of CSF 5‐HIAA are more likely to have died 4 years after sample collection than animals with relatively higher concentrations of CSF 5‐HIAA. Reproduced and adapted with permission from Higley, Mehlman, Higley, et al. (). (b) Macaque species can be categorized according to their social tolerance, varying from grade 4 (most tolerant) to grade 1 (most despotic). Reproduced and adapted with permission from Thierry (). (c) A summary figure illustrating the known relationships between diversity in serotonergic genetics, serotonergic function, social tolerance, and diversity in dominance rank, aggression, and social monitoring across species of macaques. Dotted lines represent the impact of diversity in serotonergic alleles on serotonergic function. Solid black lines represent the impact of serotonergic function on aggression, dominance status, and social tolerance. Gray lines represent the relationship between serotonergic function and social monitoring and the relationship between social monitoring and aggression, dominance status, and social tolerance
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Increasing central serotonin with 5‐HTP modulates social attention. (a) Baseline differences in how long rhesus macaques look at social and non‐social images are negatively correlated with the differences in how 40 mg/kg 5‐HTP changes looking duration to social and non‐social images relative to saline (blue dashed line). Each shape represents an individual subject's data. (b) The average differences in the changes in looking duration to social and non‐social images due to 5‐HTP for low and high baseline animals. The inset shows the raw looking duration to social (filled bars) and non‐social images (open bars) for low and high baseline animals during saline (blue) and 5‐HTP (red) sessions. Adapted and reproduced with permission from Weinberg‐Wolf et al. ()). (C) Average time courses of 5‐HTP's bi‐directional effect on attention to the mouth for low and high baseline animals. 5‐HTP increases attention to the mouth region in low baseline animals but decreases it in high baseline animals. Saline data shown in blue, and 40 mg/kg 5‐HTP in red. Adapted and reproduced with permission from Weinberg‐Wolf et al. (). (d) Average time courses of 5‐HTP's effect on attention to conspecific eyes for low and high baseline animals. While 5‐HTP has a large effect on attention to the mouth, it only modestly increases attention to the eye region in low baseline animals while modestly decreases it in high baseline animals. Saline data shown in blue and 40 mg/kg 5‐HTP in red. Adapted and reproduced with permission from Weinberg‐Wolf et al. ()
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Serotonin differentially impacts emotional recognition dependent on individual differences. (a) The SSRI citalopram (filled bars), compared to placebo (open bars), causes a bidirectional effect on fear recognition depending on whether subjects had a history of depression (red bars; decreases fear recognition due to citalopram) or were healthy volunteers (gray bars; increases fear recognition due to citalopram). Reproduced and adapted with permission from Bhagwagar et al. (). (b) ATD (filled bars versus placebo open bars) causes a bidirectional effect on the recognition of happy emotions dependent on if subjects were healthy (left graph, gray bars, an increase due to ATD) or recovered depressed (right graph, red bars, a decrease due to ATD). Reproduced and adapted with permission from Hayward et al. ()
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Social monitoring in primates differs across individuals, populations, and species. (a) Left panel: The mean frequency of positioning the body to directly face videos of non‐social stimuli, conspecifics exhibiting dominant expressions, and conspecifics exhibiting submissive expressions, for low‐, middle‐, and high‐ranking female pigtailed macaques. Right panel: The mean look duration to these same categories of videos for the same female pigtailed macaques. Middle‐ranking females faced the social videos more, and looked at the videos longer, compared to low‐ and high‐ranking females. Reproduced and adapted with permission from Capitanio et al. (). (b) While bonnet macaques living in the forest avert eye contact with conspecifics more quickly as they age, bonnet macaques living in urban environments do not. Reproduced and adapted with permission from Coss et al. (). (c) As despotic rhesus macaques age, fewer of them follow the gaze of an experimenter. Conversely, tolerant barbary macaques maintain juvenile rates of gaze following throughout their lives. Reproduced and adapted with permission from Rosati and Santos ()
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The costs and benefits of social monitoring. Primates must balance the costs and benefits associated with social monitoring. From direct‐social monitoring, primates can gain information about conspecifics fecundity and dominance status. From indirect‐social monitoring they can learn not only about fecundity and dominance status, but also environmental risk, food sources, and predation. However, monitoring others for too long can result in the social cost of unintentional aggression. It can also cause a reduction in environmental monitoring which can cause animals to learn less about environmental risk, food sources, and predation
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Neuroscience > Behavior
Psychology > Comparative Psychology
Cognitive Biology > Evolutionary Roots of Cognition
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