No evidence of attentional bias toward threatening conspecific and allospecific faces in capuchin monkeys (Sapajus [Cebus] apella) using a dot-probe task.

The ability to quickly perceive and interpret threatening facial expressions from others is critical for successfully maintaining group cohesion in social nonhuman primate species. Rapid detection of threatening or negative stimuli in the environment compared to neutral stimuli, referred to as an attentional bias toward threat, is adaptive in that faster threat detection can lead to greater survival outcomes. However, the evolutionary roots of attentional bias formation toward social threat are not well understood. The present study investigated attentional biases toward social threat and the factors associated with them, including underlying hormonal mechanisms, in socially housed capuchin monkeys. Attentional biases were assessed using a dot-probe task that measured capuchins' latency to respond to a target using a joystick after viewing threatening or neutral conspecific or allospecific faces or nonface stimuli. In our first study, we examined how age, dominance status, sex, and cortisol level related to attentional biases. In our second study, we examined how manipulated oxytocin (OT) influenced attentional biases. Capuchin monkeys did not show attentional biases toward threatening faces or objects, but they showed attentional avoidance of scrambled familiar conspecific face stimuli. Cortisol and social rank were associated with attentional bias toward threat in the capuchin monkeys that participated in this study, which suggests that stress and dominance relate to attentional bias toward social threat. Manipulated OT increased attentional avoidance of scrambled familiar and unfamiliar face images, but not unscrambled faces or objects. Overall, we did not find compelling evidence of attentional biases toward social threat in capuchin monkeys. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

Evaluation of decision-making behavior under uncertainty in capuchin monkeys (Sapajus apella) and humans (Homo sapiens) using a modified Balloon Analogue Risk Task.

Many animals, including humans, must make decisions when outcomes involve risk and/or ambiguity. To explore the evolutionary roots of decision making when outcomes are unknown, we modified the Balloon Analogue Risk Task (BART) for use with tufted capuchin monkeys (Sapajus [Cebus] apella), creating the Primate Analogue Risk Task (PART). Using both the BART and the PART, we first compared human performance across the two tasks using analogous parameters. Humans' performance on the two tasks was positively correlated. Next, we tested capuchin monkeys' performance on the PART to assess their decision-making strategies in the context of ambiguity. Secondarily, although it was not the main goal of the study, this allowed us to look at species differences between capuchins' and humans' performance. Finally, we investigated the influence of prior experience on human and capuchin decision-making behavior. Neither capuchins nor humans behaved differently following an unsuccessful trial compared to a successful trial. We found individual differences in capuchin monkeys' choice behavior, though as a whole they demonstrated a pattern of reward maximization over time. Finally, as a species, capuchins had lower PART risk scores than humans. This paradigm presents a useful way to assess behavior in a context with uncertain outcomes using a comparative approach. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Sex differences in white matter tracts of capuchin monkey brains.

Nonhuman primates exhibit sexual dimorphism in behavior, suggesting that there could be underlying differences in brain organization and function. Understanding this neuroanatomical variation is critical for enhancing our understanding of the evolution of sex differences in the human brain. Tufted capuchin monkeys (Sapajus [Cebus] apella) represent a phylogenetically diverse taxa of neotropical primates that converge on several behavioral characteristics with humans relevant to social organization, making them an important point of comparison for studying the evolution of sex differences in primates. While anatomical sex differences in gray matter have previously been found in capuchin monkeys, the current study investigates sex differences in white matter tracts. We carried out tract-based spatial statistical analysis on fractional anisotropy images of tufted capuchin monkeys (15 female, 5 male). We found that females showed significantly higher fractional anisotropy than males in regions of frontal-parietal white matter in the right cerebral hemisphere. Paralleling earlier findings in gray matter, male and female fractional anisotropy values in these regions were nonoverlapping. This complements prior work pointing toward capuchin sex differences in limbic circuitry and higher-order visual regions. We propose that these sex differences are related to the distinct socioecological niches occupied by male and female capuchins. Capuchin neuroanatomical sex differences appear to be more pronounced than in humans, which we suggest may relate to human adaptations for prolonged neurodevelopmental trajectories and increased plasticity.

Oxytocin increases during fur-rubbing regardless of level of social contact in tufted capuchin monkeys.

Social interactions induce oxytocin release in many social species, suggesting that oxytocin is a critical part of social bonding among individuals. However, oxytocin also increases as a result of physical contact and stimulation, making it unclear which features of affiliative behaviors (for instance, social interaction or physical contact with a conspecific) drive the oxytocin increase observed after engaging in these behaviors. We attempted to tease this apart by studying the differential effect of social interaction, visual coordination with a conspecific, and physical stimulation during the fur-rubbing behavior of tufted capuchin monkeys (Sapajus [Cebus] apella), which often involves social contact with groupmates but is in some cases performed alone. We induced fur-rubbing by providing onions under three conditions: when capuchins had physical access to their social group and fur-rubbed in contact with groupmates (social condition), when capuchins were separated from their social group but could still see them fur-rub (visual coordination), and when capuchins were physically and visually separated from their groupmates (physical stimulation only). We assessed urinary oxytocin in these three conditions and compared them to a control condition in which apples were provided and no fur-rubbing was observed. Capuchins fur-rubbed for less time when they could not see their groupmates, but fur-rubbing increased urinary oxytocin above the control condition in all three fur-rubbing conditions equally, suggesting that the physical stimulation derived from fur-rubbing was the most important driver of oxytocin increase. These results support a model in which physical stimulation is an important factor in the relationship between oxytocin and at least some behaviors, suggesting that oxytocin increase alone is not necessarily indicative of a social influence on behavior. Future work is needed to determine the contexts in which social factors do impact oxytocin, and whether the downstream behaviors are the same for socially and nonsocially induced oxytocin release.

Using an on-site laboratory for fecal steroid analysis in wild white-faced capuchins.

Hormone laboratories located "on-site" where field studies are being conducted have a number of advantages. On-site laboratories allow hormone analyses to proceed in near-real-time, minimize logistics of sample permits/shipping, contribute to in-country capacity-building, and (our focus here) facilitate cross-site collaboration through shared methods and a shared laboratory. Here we provide proof-of-concept that an on-site hormone laboratory (the Taboga Field Laboratory, located in the Taboga Forest Reserve, Costa Rica) can successfully run endocrine analyses in a remote location. Using fecal samples from wild white-faced capuchins (Cebus imitator) from three Costa Rican forests, we validate the extraction and analysis of four steroid hormones (glucocorticoids, testosterone, estradiol, progesterone) across six assays (DetectX® and ISWE, all from Arbor Assays). Additionally, as the first collaboration across three long-term, wild capuchin field sites (Lomas Barbudal, Santa Rosa, Taboga) involving local Costa Rican collaborators, this laboratory can serve as a future hub for collaborative exchange.

Sex differences in the brains of capuchin monkeys (Sapajus [Cebus] apella).

This study reports an analysis of 20 T1-weighted magnetic resonance imaging scans from tufted capuchin monkeys (5 male, 15 female). We carried out a data-driven, whole-brain volumetric analysis on regional gray matter anatomy using voxel-based morphometry. This revealed that males showed statistically significant expansion of a region of the hypothalamus, while females showed significant expansion in a distributed set of regions, including the cerebellum, early visual cortex, and higher-order visual regions spanning occipital and temporal cortex. In order to elucidate the network connectivity of these regions, we employed probabilistic tractography on diffusion tensor imaging data. This showed that the female-enlarged regions connect with distributed association networks across the brain. Notably, this contrasts with rodent studies, where sex differences are focused in deep, ancestral limbic regions involved in the control of reproductive behavior. Additionally, in our data set, for several regions, male and female volumetric measures were completely nonoverlapping. This contrasts with human studies, where sex differences in cortical regions have been reported but are characterized by overlapping rather than divergent male and female values. We suggest that these results can be understood in the context of the different lifetime experiences of males and females, which may produce increased experience-dependent cortical plasticity in capuchins compared to rodents, and in humans compared to capuchins.