Visual attention to facial features is an important way that group-living primate species gain knowledge about others. However, where this attention is focused on the face is influenced by contextual and social features, and emerging evidence in Pan species suggests that oxytocin, a hormone involved in forming and maintaining affiliative bonds among members of the same group, influences social attention as measured by eye gaze. Specifically, bonobos tend to focus on conspecifics’ eyes when viewing two-dimensional images, whereas chimpanzees focus more on the edges of the face. Moreover, exogenous oxytocin, which was hypothesized to increase eye contact in both species, instead enhanced this existing difference. We follow up on this to (1) determine the degree to which this Pan pattern generalizes across highly social, cooperative non-ape primates and (2) explore the impact of exogenously administered vs. endogenously released oxytocin in impacting this behavior. To do so, we tracked gaze direction on a computerized social categorization task using conspecific faces in tufted capuchin monkeys ( Sapajus [Cebus] apella ) after (1) exogenously administering intranasal oxytocin using a nebulizer or (2) inducing an endogenous increase in oxytocin using fur-rubbing, previously validated to increase oxytocin in capuchins. Overall, we did not find a general tendency in the capuchins to look toward the eyes or mouth, but we found that oxytocin was related to looking behavior toward these regions, albeit not in a straightforward way. Considering frequency of looking per trial, monkeys were more likely to look at the eye region in the fur-rubbing condition as compared to either the saline or exogenous oxytocin conditions. However, in terms of duration of looking during trials in which they did look at the eye region, monkeys spent significantly less time looking at the eyes in both oxytocin conditions as compared to the saline condition. These results suggest that oxytocin did not necessarily enhance eye looking in capuchins, which is consistent with the results from Pan species, and that endogenous and exogenous oxytocin may behave differently in their effect on how social attention is allocated.
more »
« less
Conserved and differing functions of the endocrine system across different social systems – oxytocin as a case study
A key goal of the field of endocrinology has been to understand the hormonal mechanisms that drive social behavior and influence reactions to others, such as oxytocin. However, it has sometimes been challenging to understand which aspects and influences of hormonal action are conserved and common among mammalian species, and which effects differ based on features of these species, such as social system. This challenge has been exacerbated by a focus on a relatively small number of traditional model species. In this review, we first demonstrate the benefits of using non-traditional models for the study of hormones, with a focus on oxytocin as a case study in adding species with diverse social systems. We then expand our discussion to explore differing effects of oxytocin (and its response to behavior) within a species, with a particular focus on relationship context and social environment among primate species. Finally, we suggest key areas for future exploration of oxytocin’s action centrally and peripherally, and how non-traditional models can be an important resource for understanding the breadth of oxytocin’s potential effects.
more »
« less
- Award ID(s):
- 1919305
- PAR ID:
- 10528890
- Publisher / Repository:
- Frontiers
- Date Published:
- Journal Name:
- Frontiers in Endocrinology
- Volume:
- 15
- ISSN:
- 1664-2392
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
null (Ed.)Oxytocin increases the salience of both positive and negative social contexts and it is thought that these diverse actions on behavior are mediated in part through circuit-specific action. This hypothesis is based primarily on manipulations of oxytocin receptor function, leaving open the question of whether different populations of oxytocin neurons mediate different effects on behavior. Here we inhibited oxytocin synthesis in a stress-sensitive population of oxytocin neurons specifically within the medioventral bed nucleus of the stria terminalis (BNSTmv). Oxytocin knockdown prevented social stress-induced increases in social vigilance and decreases in social approach. Viral tracing of BNSTmv oxytocin neurons revealed fibers in regions controlling defensive behaviors, including lateral hypothalamus, anterior hypothalamus, and anteromedial BNST (BNSTam). Oxytocin infusion into BNSTam in stress naïve mice increased social vigilance and reduced social approach. These results show that a population of extrahypothalamic oxytocin neurons plays a key role in controlling stress-induced social anxiety behaviors.more » « less
-
Carbon fiber microelectrodes (CFMEs) have been used to detect neurotransmitters and other biomolecules using fast-scan cyclic voltammetry (FSCV) for the past few decades. This technique measures neurotransmitters such as dopamine and, more recently, physiologically relevant neuropeptides. Oxytocin, a pleiotropic peptide hormone, is physiologically important for adaptation, development, reproduction, and social behavior. This neuropeptide functions as a stress-coping molecule, an anti-inflammatory agent, and serves as an antioxidant with protective effects especially during adversity or trauma. Here, we measure tyrosine using the Modified Sawhorse Waveform (MSW), enabling enhanced electrode sensitivity for the amino acid and oxytocin peptide. Applying the MSW, decreased surface fouling and enabled codetection with other monoamines. As oxytocin contains tyrosine, the MSW was also used to detect oxytocin. The sensitivity of oxytocin detection was found to be 3.99 ± 0.49 nAμM−1, (n = 5). Additionally, we demonstrate that applying the MSW on CFMEs allows for real time measurements of exogenously applied oxytocin on rat brain slices. These studies may serve as novel assays for oxytocin detection in a fast, sub-second timescale with possible implications forin vivomeasurements and further understanding of the physiological role of oxytocin.more » « less
-
The nonapeptide system modulates numerous social behaviors through oxytocin and vasopressin activation of the oxytocin receptor (OXTR) and vasopressin receptor (AVPR1A) in the brain. OXTRs and AVPR1As are widely distributed throughout the brain and binding densities exhibit substantial variation within and across species. Although OXTR and AVPR1A binding distributions have been mapped for several rodents, this system has yet to be characterized in the spiny mouse (Acomys cahirinus). Here we conducted receptor autoradiography and in situ hybridization to map distributions of OXTR and AVPR1A binding and Oxtr and Avpr1a mRNA expression throughout the basal forebrain and midbrain of male and female spiny mice. We found that nonapeptide receptor mRNA is diffuse throughout the forebrain and midbrain and does not always align with OXTR and AVPR1A binding. Analyses of sex differences in brain regions involved in social behavior and reward revealed that males exhibit higher OXTR binding densities in the lateral septum, bed nucleus of the stria terminalis, and anterior hypothalamus. However, no association with gonadal sex was observed for AVPR1A binding. Hierarchical clustering analysis further revealed that co-expression patterns of OXTR and AVPR1A binding across brain regions involved in social behavior and reward differ between males and females. These findings provide mapping distributions and sex differences in nonapeptide receptors in spiny mice. Spiny mice are an excellent organism for studying grouping behaviors such as cooperation and prosociality, and the nonapeptide receptor mapping here can inform the study of nonapeptide-mediated behavior in a highly social, large group-living rodent.more » « less
-
null (Ed.)In the past decade, there has been a surge of interest in using games derived from experimental economics to test decision-making behaviour across species. In most cases, researchers are using the games as a tool, for instance, to understand what factors influence decision-making, how decision-making differs across species or contexts, or to ask broader questions about species’ propensities to cooperate or compete. These games have been quite successful in this regard. To what degree, however, do these games tap into species' economic decision-making? For the purpose of understanding the evolution of economic systems in humans, this is the key question. To study this, we can break economic decision-making down into smaller components, each of which is a potential step in the evolution of human economic behaviour. We can then use data from economic games, which are simplified, highly structured models of decision-making and therefore ideal for the comparative approach, to directly compare these components across species and contexts, as well as in relation to more naturalistic behaviours, to better understand the evolution of economic behaviour and the social and ecological contexts that influenced it. The comparative approach has successfully informed us about the evolution of other complex traits, such as language and morality, and should help us more deeply understand why and how human economic systems evolved. This article is part of the theme issue ‘Existence and prevalence of economic behaviours among non-human primates’.more » « less
An official website of the United States government

