Abstract
BackgroundSerotonin signaling influences social behavior in both human and nonhuman primates. In humans, variation upstream of the promoter region of the serotonin transporter gene (5-HTTLPR) has recently been shown to influence both behavioral measures of social anxiety and amygdala response to social threats. Here we show that length polymorphisms in 5-HTTLPR predict social reward and punishment in rhesus macaques, a species in which 5-HTTLPR variation is analogous to that of humans.Methodology/Principal FindingsIn contrast to monkeys with two copies of the long allele (L/L), monkeys with one copy of the short allele of this gene (S/L) spent less time gazing at face than non-face images, less time looking in the eye region of faces, and had larger pupil diameters when gazing at photos of a high versus low status male macaques. Moreover, in a novel primed gambling task, presentation of photos of high status male macaques promoted risk-aversion in S/L monkeys but promoted risk-seeking in L/L monkeys. Finally, as measured by a “pay-per-view” task, S/L monkeys required juice payment to view photos of high status males, whereas L/L monkeys sacrificed fluid to see the same photos.Conclusions/SignificanceThese data indicate that genetic variation in serotonin function contributes to social reward and punishment in rhesus macaques, and thus shapes social behavior in humans and rhesus macaques alike.
Highlights
The synaptic serotonin transporter plays a crucial role in regulating emotion in both human and non-human primates
Post-hoc ttests revealed that short allele (S/L) monkeys chose the risky option significantly less often than the long allele (L/L) monkeys did when primed with an image of a high status male face (LSD t-test, df = 475, p = 0.0005), whereas there were no significant differences between S/L and L/ L animals for the other three image categories ((gray square, p = 0.54; subordinate face, p = 0.53, perinea, p = 0.24; Figure 3A)
We found that rhesus monkeys carrying the short allele (S/L) were less likely than monkeys homozygous for the long allele (L/L) to gaze directly at the faces and eyes of conspecifics, and that they exhibit a larger sympathetic response, as measured by pupil dilation, to images of high status individuals
Summary
The synaptic serotonin transporter plays a crucial role in regulating emotion in both human and non-human primates. Functional imaging studies indicate that human S carriers exhibit enhanced amygdala response to social threats such as angry faces [7,8] Based on these observations, we predicted that allelic variation in 5-HTTPLR would influence individual reactivity to social reward and punishment in rhesus macaques, as it appears to do in humans. We predicted that allelic variation in 5-HTTPLR would influence individual reactivity to social reward and punishment in rhesus macaques, as it appears to do in humans We tested this hypothesis in three complimentary experiments: First, we measured eye gaze patterns and pupil diameter in male rhesus macaques when they were given the opportunity to look at images of other rhesus macaques; second, we measured the effects of seeing social images on subsequent gambling for juice rewards; and third, we measured the amount of juice male rhesus macaques sacrificed or demanded for the opportunity to see these images. These experiments provide three implicit measures of the influence of social stimuli on neural systems mediating reward and punishment [9,10,11]
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