No abstract

Animals that maintain cooperative relationships show gains in longevity and offspring survival. However, little is known about the cognitive or hormonal mechanisms involved in cooperation. Indeed, there is little support for a main hypothesis that non-human animals have the cognitive capacities required for bookkeeping of cooperative exchanges. We tested an alternative hypothesis that cooperative relationships are facilitated by an endocrinological mechanism involving oxytocin, a hormone required for bonding in parental and sexual relationships across mammals. We measured urinary oxytocin after single bouts of grooming in wild chimpanzees. Oxytocin levels were higher after grooming with bond partners compared with nonbond partners or after no grooming, regardless of genetic relatedness or sexual interest. We ruled out other possible confounds, such as grooming duration, grooming direction or sampling regime issues, indicating that changes in oxytocin levels were mediated by social bond strength. Oxytocin, which is thought to act directly on neural reward and social memory systems, is likely to play a key role in keeping track of social interactions with multiple individuals over time. The evolutionary linkage of an ancestral hormonal system with complex social cognition may be the primary mechanism through which long-term cooperative relationships develop between both kin and non-kin in mammals.

Oxytocin (OT) is a neuropeptide that is produced primarily in the hypothalamus and is best known for its role in mammalian birth and lactation. Recent evidence also implicates OT in social behaviors, including parental behavior, the formation of social bonds, and the management of stressful experiences. OT is reactive to stressors, and plays a role in the regulation of both the central and autonomic nervous system, including effects on immune and cardiovascular function. Knowledge of patterns of OT release would be of value in many fields of science and medicine. However, measurements of OT concentration in blood are infrequently performed, and previous attempts to measure OT in saliva have been unsuccessful. Using a sensitive enzyme immunoassay (EIA) and concentrated samples we were able to detect reproducible changes in salivary OT as a function of lactation and massage. These results indicate that measurements of biologically relevant changes in salivary OT are possible. These results confirm the biological relevance of changes in salivary OT with stressors and support saliva as a noninvasive source to monitor central neuroendocrine function.

The formation of social attachments is a critical component of human relationships. Infants begin to bond to their caregivers from the moment of birth, and these social bonds continue to provide regulatory emotional functions throughout adulthood. It is difficult to examine the interactions between social experience and the biological origins of these complex behaviors because children undergo both brain development and accumulate social experience at the same time. We had a rare opportunity to examine children who were reared in extremely aberrant social environments where they were deprived of the kind of care-giving typical for our species. The present experiment in nature provides insight into the role of early experience on the brain systems underlying the development of emotional behavior. These data indicate that the vasopressin and oxytocin neuropeptide systems, which are critical in the establishment of social bonds and the regulation of emotional behaviors, are affected by early social experience. The results of this experiment suggest a potential mechanism whose atypical function may explain the pervasive social and emotional difficulties observed in many children who have experienced aberrant care-giving. The present findings are consistent with the view that there is a critical role for early experience in the development of the brain systems underlying basic aspects of human social behavior.attachment ͉ emotion ͉ oxytocin ͉ vasopressin ͉ child abuse T he social attachments formed between human infants and their caregivers begin very early in postnatal life and play a critical role in children's survival and healthy adaptation. Typically, adults provide infants with a social environment that is fairly consistent. Caregivers learn how to recognize and respond to the infants' needs, thereby creating predictable contingencies in the environment; these regularities, in turn, make the infant's environment secure and conducive to further social learning (1, 2). Multiple perceptual, sensory, cognitive, and affective systems must become synchronized so that a social bond can develop between an infant and caregiver; this bond is then reflected in the child's adaptive behavioral responses to the environment. The goal of this experiment was to address a fundamental evolutionary and developmental question: To what extent are the neurobiological systems that regulate affiliative behaviors dependent on the social experiences afforded to most infants by their caregivers?It is difficult to evaluate the effects of early social experience on the organization of the developing brain because, within seconds of postnatal life, the human infant experiences a vast amount of emotional input. In this regard, the maturation of the brain is confounded with the accumulation of social experience. One way to address this problem is to experimentally manipulate the social environment. Although this approach is successful with nonhuman animals, such studies are neither possible nor desirable to undertake with human children. There...

The common marmoset (Callithrix jacchus) is poised to become a standard nonhuman primate aging model. With an average lifespan of 5 to 7 years and a maximum lifespan of 16.5 years, marmosets are the shortest-lived anthropoid primates. They display age-related changes in pathologies that mirror those seen in humans, such as cancer, amyloidosis, diabetes, and chronic renal disease. They also display predictable age-related differences in lean mass, calf circumference, circulating albumin, hemoglobin, and hematocrit. Features of spontaneous sensory and neurodegenerative change—for example, reduced neurogenesis, β-amyloid deposition in the cerebral cortex, loss of calbindin D28k binding, and evidence of presbycusis—appear between the ages of 7 and 10 years. Variation among colonies in the age at which neurodegenerative change occurs suggests the interesting possibility that marmosets could be specifically managed to produce earlier versus later occurrence of degenerative conditions associated with differing rates of damage accumulation. In addition to the established value of the marmoset as a model of age-related neurodegenerative change, this primate can serve as a model of the integrated effects of aging and obesity on metabolic dysfunction, as it displays evidence of such dysfunction associated with high body weight as early as 6 to 8 years of age.

Vocalizations are important components of social behaviour in many vertebrate species, including our own. Less well-understood are the hormonal mechanisms involved in response to vocal cues, and how these systems may influence the course of behavioural evolution. The neurohormone oxytocin (OT) partly governs a number of biological and social processes critical to fitness, such as attachment between mothers and their young, and suppression of the stress response after contact with trusted conspecfics. Rodent studies suggest that OT's release is contingent upon direct tactile contact with such individuals, but we hypothesized that vocalizations might be capable of producing the same effect. To test our hypothesis, we chose human mother -daughter dyads and applied a social stressor to the children, following which we randomly assigned participants into complete contact, speech-only or no-contact conditions. Children receiving a full complement of comfort including physical, vocal and non-verbal contact showed the highest levels of OT and the swiftest return to baseline of a biological marker of stress (salivary cortisol), but a strikingly similar hormonal profile emerged in children comforted solely by their mother's voice. Our results suggest that vocalizations may be as important as touch to the neuroendocrine regulation of social bonding in our species.

Humans excel in cooperative exchanges between unrelated individuals. Although this trait is fundamental to the success of our species, its evolution and mechanisms are poorly understood. Other social mammals also build long-term cooperative relationships between non-kin, and recent evidence shows that oxytocin, a hormone involved in parent-offspring bonding, is likely to facilitate non-kin as well as kin bonds. In a population of wild chimpanzees, we measured urinary oxytocin levels following a rare cooperative event-food sharing. Subjects showed higher urinary oxytocin levels after single food-sharing events compared with other types of social feeding, irrespective of previous social bond levels. Also, urinary oxytocin levels following food sharing were higher than following grooming, another cooperative behaviour. Therefore, food sharing in chimpanzees may play a key role in social bonding under the influence of oxytocin. We propose that food-sharing events co-opt neurobiological mechanisms evolved to support mother-infant bonding during lactation bouts, and may act as facilitators of bonding and cooperation between unrelated individuals via the oxytocinergic system across social mammals.

Identifying factors that influence animal density is a fundamental goal in ecology that has taken on new importance with the need to develop informed management plans. This is particularly the case for primates as the tropical forest that supports many species is being rapidly converted. We use a system of forest fragments adjacent to Kibale National Park, Uganda, to examine if food availability and parasite infections have synergistic affects on red colobus (Piliocolobus tephrosceles) abundance. Given that the size of primate populations can often respond slowly to environmental changes, we also examined how these factors influenced cortisol levels. To meet these objectives, we monitored gastrointestinal parasites, evaluated fecal cortisol levels, and determined changes in food availability by conducting complete tree inventories in eight fragments in 2000 and 2003. Red colobus populations declined by an average of 21% among the fragments; however, population change ranged from a 25% increase to a 57% decline. The cumulative basal area of food trees declined by an average of 29.5%; however, forest change was highly variable (a 2% gain to a 71% decline). We found that nematode prevalence averaged 58% among fragments (range 29-83%). The change in colobus population size was correlated both with food availability and a number of indices of parasite infections. A path analysis suggests that change in food availability has a strong direct effect on population size, but it also has an indirect effect via parasite infections.