Michael L. Platt

Differences in feeding ecology predict differences in performance between golden lion tamarins (Leontopithecus rosalia) and Wied's marmosets (Callithrix kuhli) on spatial and visual memory tasks

Golden lion tamarins (Leontopithecus rosalia) and Wied’s marmosets (Callithrix kuhli) exhibited adaptive differences in performance on several distinct memory tasks. On both an open-field analogue of a radial arm maze and a spatial delayed matching-to-sample task, the marmosets performed better than the tamarins after short (5-min) retention intervals, but only the tamarins continued to perform above chance after long (24- or 48-h) retention intervals. The marmosets also required less training than the tamarins did to learn a color memory task, but again only the tamarins performed above chance when the retention interval was increased to 24 h. The results of these experiments are consistent with predictions based on knowledge of the feeding ecology of these species in the wild and raise the possibility that they possess different visuospatial memory abilities specialized for tracking the spatial and temporal distribution of their principal foods.

Family network size and survival across the lifespan of female macaques

Two decades of research suggest social relationships have a common evolutionary basis in humans and other gregarious mammals. Critical to the support of this idea is growing evidence that mortality is influenced by social integration, but when these effects emerge and how long they last is mostly unknown. Here, we report in adult female macaques that the impact of number of close adult female relatives, a proxy for social integration, on survival is not experienced uniformly across the life course; prime-aged females with a greater number of relatives had better survival outcomes compared with prime-aged females with fewer relatives, whereas no such effect was found in older females. Group size and dominance rank did not influence this result. Older females were less frequent targets of aggression, suggesting enhanced experience navigating the social landscape may obviate the need for social relationships in old age. Only one study of humans has found age-based dependency in the association between social integration and survival. Using the largest dataset for any non-human animal to date, our study extends support for the idea that sociality promotes survival and suggests strategies employed across the life course change along with experience of the social world.

Increased reward value of non-social stimuli in children and adolescents with autism.

An econometric choice task was used to estimate the implicit reward value of social and non-social stimuli related to restricted interests in children and adolescents with (n = 12) and without (n = 22) autism spectrum disorder (ASD). Mixed effects logistic regression analyses revealed that groups differed in valuation of images related to restricted interests: control children were indifferent to cash payouts to view these images, but children with ASD were willing to receive less cash payout to view these images. Groups did not differ in valuation of social images or non-social images not related to restricted interests. Results highlight that motivational accounts of ASD should also consider the reward value of non-social stimuli related to restricted interests in ASD (Dichter and Adolphs, 2012).

Eye and head movements shape gaze shifts in Indian peafowl

ABSTRACT Animals selectively direct their visual attention toward relevant aspects of their environments. They can shift their attention using a combination of eye, head and body movements. While we have a growing understanding of eye and head movements in mammals, we know little about these processes in birds. We therefore measured the eye and head movements of freely behaving Indian peafowl (Pavo cristatus) using a telemetric eye-tracker. Both eye and head movements contributed to gaze changes in peafowl. When gaze shifts were smaller, eye movements played a larger role than when gaze shifts were larger. The duration and velocity of eye and head movements were positively related to the size of the eye and head movements, respectively. In addition, the coordination of eye and head movements in peafowl differed from that in mammals; peafowl exhibited a near-absence of the vestibulo-ocular reflex, which may partly result from the peafowls ability to move their heads as quickly as their eyes. Summary: Indian peafowl use eye and head movements to shift their gaze but, unlike mammals, they do not rely on the vestibulo-ocular reflex to stabilize their gaze.

Oxytocin and vasopressin flatten dominance hierarchy and enhance behavioral synchrony in part via anterior cingulate cortex

The neuropeptides oxytocin (OT) and arginine vasopressin (AVP) influence social functions in many mammals. In humans and rhesus macaques, OT delivered intranasally can promote prosocial behavior in certain contexts. Yet the precise neural mechanisms mediating these behavioral effects remain unclear. Here we show that treating a group of male macaque monkeys intranasally with aerosolized OT relaxes their spontaneous social interactions with other monkeys. OT reduces differences in social behavior between dominant and subordinate monkeys, thereby flattening the status hierarchy. OT also increases behavioral synchrony within a pair. Intranasal delivery of aerosolized AVP reproduces the effects of OT with greater efficacy. Remarkably, all behavioral effects are replicated when OT or AVP is injected focally into the anterior cingulate gyrus (ACCg), a brain area linked to empathy and other-regarding behavior. ACCg lacks OT receptors but is rich in AVP receptors, suggesting exogenous OT may shape social behavior, in part, via nonspecific binding. Notably, OT and AVP alter behaviors of both the treated monkey and his untreated partner, consistent with enhanced feedback through reciprocal social interactions. These findings bear important implications for use of OT in both basic research and as a therapy for social impairments in neurodevelopmental disorders.

Posterior Cingulate Neurons Dynamically Signal Decisions to Disengage during Foraging

Foraging for resources is a fundamental behavior balancing systematic search and strategic disengagement. The foraging behavior of primates is especially complex and requires long-term memory, value comparison, strategic planning, and decision-making. Here we provide evidence from two different foraging tasks that neurons in primate posterior cingulate cortex (PCC) signal decision salience during foraging to motivate disengagement from the current strategy. In our foraging tasks, salience refers to the difference between decision thresholds and the net harvested reward. Salience signals were stronger in poor foraging contexts than rich ones, suggesting low harvest rates recruit mechanisms in PCC that regulate strategic disengagement and exploration during foraging.

Weak effects of common genetic variation in oxytocin and vasopressin receptor genes on rhesus macaque social behavior

The neuropeptides oxytocin (OT) and arginine vasopressin (AVP) influence pair bonding, attachment, and sociality, as well as anxiety and stress responses in humans and other mammals. The effects of these peptides are mediated by genetic variability in their associated receptors, OXTR and the AVPR gene family. However, the role of these genes in regulating social behaviors in non‐human primates is not well understood. To address this question, we examined whether genetic variation in the OT receptor gene OXTR and the AVP receptor genes AVPR1A and AVPR1B influence naturally‐occurring social behavior in free‐ranging rhesus macaques—gregarious primates that share many features of their biology and social behavior with humans. We assessed rates of social behavior across 3,250 hr of observational behavioral data from 201 free‐ranging rhesus macaques on Cayo Santiago island in Puerto Rico, and used genetic sequence data to identify 25 OXTR, AVPR1A, and AVPR1B single‐nucleotide variants (SNVs) in the population. We used an animal model to estimate the effects of 12 SNVs (n = 3 OXTR; n = 5 AVPR1A; n = 4 AVPR1B) on rates of grooming, approaches, passive contact, contact aggression, and non‐contact aggression, given and received. Though we found evidence for modest heritability of these behaviors, estimates of effect sizes of the selected SNVs were close to zero, indicating that common OXTR and AVPR variation contributed little to social behavior in these animals. Our results are consistent with recent findings in human genetics that the effects of individual common genetic variants on complex phenotypes are generally small.

Rhesus Macaques Form Preferences for Brand Logos Through Sex and Social Status Based Advertising

Like humans, monkeys value information about sex and status, inviting the hypothesis that our susceptibility to these factors in advertising arises from shared, ancestral biological mechanisms that prioritize social information. To test this idea, we asked whether rhesus macaques (Macaca mulatta) show choice behavior that is similar to humans in response to sex and social status in advertising. Our results show that monkeys form preferences for brand logos repeatedly paired with images of macaque genitals and high status monkeys. Moreover, monkeys sustain preferences for these brand logos even though choosing them provided no tangible rewards, a finding that cannot be explained by a decision mechanism operating solely on material outcomes. Together, our results endorse the hypothesis that the power of sex and status in advertising emerges from the spontaneous engagement of shared, ancestral neural circuits that prioritize information useful for navigating the social environment. Finally, our results show that simple associative conditioning is sufficient to explain the formation of preferences for brand logos paired with sexual or status-based images.

Opportunities and challenges for intranasal oxytocin treatment studies in nonhuman primates

Nonhuman primates provide a human‐relevant experimental model system to explore the mechanisms by which oxytocin (OT) regulates social processing and inform its clinical applications. Here, we highlight contributions of the nonhuman primate model to our understanding of OT treatment and address unique challenges in administering OT to awake behaving primates. Prior preclinical research utilizing macaque monkeys has demonstrated that OT can modulate perception of other individuals and their expressions, attention to others, imitation, vigilance to social threats, and prosocial decisions. We further describe ongoing efforts to develop an OT delivery system for use in experimentally naïve juvenile macaque monkeys compatible with naturalistic social behavior outcomes. Finally, we discuss future directions to further develop the rhesus monkey as a preclinical test bed to evaluate the effects of OT exposure and advance efforts to translate basic science OT research into safe and effective OT therapies.

Persistent social isolation reflects identity and social context but not maternal effects or early environment

Individuals who are well integrated into society have greater access to resources and tend to live longer. Why some individuals are socially isolated and others are not is therefore puzzling from an evolutionary perspective. Answering this question requires establishing the mix of intrinsic and contextual factors that contribute to social isolation. Using social network data spanning up to half of the median adult lifespan in a gregarious primate, we found that some measures of social isolation were modestly repeatable within individuals, consistent with a trait. By contrast, social isolation was not explained by the identity of an animal’s mother or the group into which it was born. Nevertheless, age, sex and social status each played a role, as did kin dynamics and familiarity. Females with fewer close relatives were more isolated, and the more time males spent in a new group the less isolated they became, independent of their social status. These results show that social isolation results from a combination of intrinsic and environmental factors. From an evolutionary perspective, these findings suggest that social isolation could be adaptive in some contexts and partly maintained by selection.