Behavior In Nonhuman Primates Research Articles

Human–Ape Interactions in a Zoo Setting: Gorillas and Orangutans Modify Their Behavior Depending upon Human Familiarity

ABSTRACTUnderstanding how human presence influences animal behavior, specifically the behavior of nonhuman primates, has important implications for methodology in cognitive and behavioral studies, for our understanding of human–animal relationships and for animal welfare in captive settings. Conducted in the San Diego Zoo, this study partially replicates an existing study on human–animal relationships, which focused on familiarity effects on the human-directed behavior of great apes residing in the Toronto Zoo. Such a replication in a new location and with different individuals is necessary to expand sample size and to better understand how ontogeny and living environment influence human-directed ape behavior. All-occurrence sampling of human-directed behavior was used to gather data on two gorilla groups and one orangutan group, all housed at the San Diego Zoo. The aim was to compare ape-initiated behaviors toward zoo staff with apeinitiated visitor-directed behavior, in accordance with predictions of the Human–Animal Relationship (HAR) model. Overall, human-directed behaviors were more frequent toward visitors than toward staff, mainly caused by increased visitor-directed visual behavior, specifically brief glances. Given that visual monitoring has been seen as fearful behavior, potentially related to predator monitoring, this would confirm the expectation that lack of familiarity will lead to increased visual vigilance. However, the visitor-directed visual behaviors may not be antagonistic or fearful. Considering the specific behaviors and exhibit designs, curiosity may be an equally likely explanation in this context. Aiming to also understand whether these groups exhibited species differences in human-directed behavior, it was found that orangutans engaged in more affiliative behavior overall than gorillas. Comparing our results with the previous study, we conclude that while effects of familiarity are present, those effects are modulated by both individual ontogeny and exhibit design. While the HAR model is partially supported, additional factors may need to be included to fully interpret the observed behavior. Additional research is needed to further understand the effects of species, sex, and ontogeny on the predictions of the HAR model.

Fibroblast growth factor 21: an endocrine inhibitor of sugar and alcohol appetite.

Fibroblast growth factor 21 (FGF21) is a liver-derived hormone with pleiotropic metabolic effects. Its production is induced by various dietary imbalances in mice (including low-protein and ketogenic diets, fructose feeding and ethanol), hinting that it might influence food preference given the role of the liver in maintaining homeostatic levels of circulating nutrients. In 2016, it was shown that FGF21 selectively inhibits consumption of sugars and the primary product of their fermentation, ethanol, but not intake of fat, protein or complex carbohydrates. Since then, studies have sought to unravel this selectivity, its physiological purpose and translational relevance, as well as delineate the neural mechanisms involved. Initially found to impact ingestive behaviours in mice and non-human primates, FGF21 is also induced in humans by sugars and, far more dramatically, by acute alcohol intake. Genetic studies have revealed that patterns of weekly candy and alcohol consumption are associated with genetic variants in FGF21 and its co-receptor β-klotho (KLB), suggesting that liking for sugar, and fermented sugar, may be influenced by natural variation in FGF21 signal strength in humans. Herein, we discuss our nascent understanding of FGF21 as a selective negative regulator of sugar and alcohol appetite as well as reasons why such a peculiar system may have evolved in mammals. Uncovering the regulatory network governing sugar, and fermented sugar, intake could provide new opportunities to improve dietary choices in a population suffering from Western diet-induced diseases fuelled in part by a runaway sweet - and alcohol - tooth.

Dopamine D1-like receptors regulate agonistic components of pair bond maintenance behaviors in male titi monkeys (Callicebus cupreus)

Several neurobiological mechanisms are implicated in the formation of selective pair bonds in socially monogamous mammals, however much less is known about the mechanisms that underlie the long-term behavioral maintenance of these bonds. In prairie voles (Microtus ochrogaster), agonistic behavior that contributes to pair bond maintenance are regulated by dopamine activity at D1-like receptors (D1R) within the mesocorticolimbic system. Evidence suggests D1Rs similarly regulate the behavioral components of pair bond maintenance in socially monogamous titi monkeys (Callicebus cupreus); however, evaluation with behavioral pharmacology is necessary to evaluate this hypothesis. In the current study we evaluated the role of D1Rs in behavioral components of pair bond maintenance in captive male titi monkeys (N = 8). We administered two doses of a D1R selective antagonist, SCH23390, (0.1 mg/kg, 0.01 mg/kg) or saline vehicle to male titi monkeys and presented pairs with a simulated intruder monkey via the use of a mirror stimulus. The non-reflective back of the mirror stimulus was used for control sessions. We video recorded responses to the five-minute stimulus presentations and later scored for arousal and agonistic behaviors relevant to mate guarding as well as affiliative behavior between the pair mates. We also conducted a locomotor assessment to evaluate the potential side effect for SCH23390 of impaired locomotion. Finally, we collected blood samples at the end of each session to assay for plasma cortisol responses. We found evidence of locomotor impairment only with the high dose of SCH23390, and therefore analyses were conducted comparing only test sessions where low dose SCH23390 and saline were administered. With saline administration, males displayed more agonistic behavior via back arching and tail lashing as well as restraining their female partners when viewing the mirror compared to the back of the mirror. D1R antagonist treatment attenuated these agonistic behaviors indicative of mate guarding when males viewed the mirror. Results also indicated that this reduction in agonistic behavior occurred without evidence of overall behavioral blunting or generally reduced social interest. Likewise changes in agonistic behavior were not driven by differences in HPA activity across testing sessions. Mate-directed affiliative behavior, including lip smacks and approaches to female partners, were not altered by D1R antagonist treatment. Dyadic social contact was higher with D1R antagonist treatment, but this was due to a reduction in contact termination by the treated males, which was typically followed by an approach or arousal display to the simulated intruder. These results provide further evidence that D1R activity regulates mate guarding behaviors in titi monkeys and suggests that the dopamine system plays a similar role in the agonistic behavioral components of pair bond maintenance behavior in non-human primates and rodents.

Food Craving, Seeking, and Consumption Behaviors: Conceptual Phases and Assessment Methods Used in Animal and Human Studies.

What drives us to eat? It is one of the most fundamental questions in the obesity research field which have been investigated for centuries. Numerous novel in vivo technologies in the neuroscience field allows us to reevaluate the multiple components and phases of food-related behaviors. Focused on the cognitive, executive, behavioral and temporal aspects, food-related behaviors can be distinguished into appetitive phase (food craving→food seeking) and consummatory phase (food consumption). Food craving phase is an internal state or stage in which the animal has the motivation to eat the food but there is no actual food specific behaviors or actions. Food seeking phase entails repeated behaviors with a food searching purpose until the animal discovers the food (or food-related cue) and the approach behavior stage after the discovery of food. Food consumption phase is the step that the animal grabs, chews and intake the food. This review will specifically focus on characteristics and evaluation methods for each phase of food-related behavior in rodent, non-human primates and human.

Origins of the Human Predatory Pattern: The Transition to Large-Animal Exploitation by Early Hominins

The habitual consumption of large-animal resources (e.g., similar sized or larger than the consumer) separates human and nonhuman primate behavior. Flaked stone tool use, another important hominin behavior, is often portrayed as being functionally related to this by the necessity of a sharp edge for cutting animal tissue. However, most research on both issues emphasizes sites that postdate ca. 2.0 million years ago. This paper critically examines the theoretical significance of the earlier origins of these two behaviors, their proposed interrelationship, and the nature of the empirical record. We argue that concepts of meat-eating and tool use are too loosely defined: outside-bone nutrients (e.g., meat) and inside-bone nutrients (e.g., marrow and brains) have different macronutrient characteristics (protein vs. fat), mechanical requirements for access (cutting vs. percussion), search, handling and competitive costs, encounter rates, and net returns. Thus, they would have demanded distinct technological and behavioral solutions. We propose that the regular exploitation of large-animal resources—the “human predatory pattern”—began with an emphasis on percussion-based scavenging of inside-bone nutrients, independent of the emergence of flaked stone tool use. This leads to a series of empirical test implications that differ from previous “meat-eating” origins scenarios.

CTBS increases the frequency of narrow-band gamma bursts in the contralateral pre-frontal cortex in a primate model of rTMS

Repetitive modes of TMS (rTMS) modulate behaviour in both humans and non-human primates (NHP). Although widely used in basic and clinical neuroscience, a precise understanding of the neurophysiological effects of rTMS in brain networks, and how such effects influence behaviour, is largely lacking. To overcome this gap, we study a NHP model of rTMS, focusing on the well-studied oculomotor network. Here, we report the effects of continuous theta-burst-stimulation (cTBS) to the right prefrontal cortex (PFC) on neuronal activity in the left PFC during performance of an oculomotor task.

Disturbance of approach-avoidance behaviors in non-human primates by stimulation of the limbic territories of basal ganglia and anterior insula.

The basal ganglia (BG) are involved in motivation and goal-directed behavior. Recent studies suggest that limbic territories of BG not only support reward seeking (appetitive approach) but also the encoding of aversive conditioned stimuli (CS) and the production of aversive-related behaviors (avoidance or escape). This study aimed to identify inside two BG nuclei, the striatum and pallidum, the territories involved in aversive behaviors and to compare the effects of stimulating these territories to those resulting from stimulation of the anterior Insula (aIns), a region that is well-known to be involved in aversive encoding and associated behaviors. Two monkeys performed an approach/avoidance task in which they had to choose a behavior (approach or avoidance) in an appetitive (reward) or aversive (air-puff) context. During this task, either one (single-cue) or two (dual-cue) CS provided essential information about which context-adapted behavior should be selected. Microstimulation was applied during the CS presentation. Stimulation generally reduced approaches in the appetitive contexts and increased escape behaviors (premature responses) and/or passive avoidance (noninitiated action) in aversive context. These effects were more pronounced in ventral parts of all examined structures, with significant differences observed between stimulated structures. Thresholds to induce effects were lowest in the pallidum. Striatal stimulation led to the largest diversity of effects, with a subregion even leading to enhanced active avoidance. Finally, aIns stimulations produced stronger effects in the dual-cue context. These results provide causal evidence that limbic territories of BG, like aIns, play crucial roles in the selection of context-motivated behaviors.

Saccadic momentum and attentive control in V4 neurons during visual search.

Saccadic momentum refers to the increased probability of making a saccade in a forward direction relative to the previous saccade. During visual search and free viewing conditions saccadic probability falls in a gradient from forward to backward directions. It has been considered to reflect an oculomotor bias for a continuing motor plan. Here we report that a saccadic momentum gradient is observed in nonhuman primate behavior and in the visual responses of cortical area V4 neurons during a conjunction style visual search task. This result suggests that saccadic momentum arises in part from a biased spatial distribution of visual responses to stimuli. The effect is independent of feature-based selective attention and overridden by directed spatial attention. The implications of saccadic momentum for search guidance are much broader and robust than the inhibition-of-return's presumed role in preventing refixation of recent locations.

Suppressing Effect of Baclofen on Multiple Alcohol-Related Behaviors in Laboratory Animals.

This paper summarizes the several lines of experimental evidence demonstrating the ability of the prototypic GABAB receptor agonist, baclofen, to suppress multiple alcohol-related behaviors in laboratory rodents and non-human primates exposed to validated experimental models of alcohol use disorder (AUD). Specifically, treatment with baclofen has repeatedly been reported to suppress alcohol-induced locomotor stimulation, alcohol drinking (including binge- and relapse-like drinking), operant oral alcohol self-administration, alcohol seeking, and reinstatement of alcohol seeking in rats and mice. Treatment with baclofen also reduced operant oral alcohol self-administration in baboons. Several of these effects appear to be mediated by GABAB receptors located in the ventral tegmental area. The often observed co-occurrence of “desired” pharmacological effects and “unwanted” sedative effects represents the major drawback of the preclinical, anti-alcohol profile of baclofen. Collectively, these data underline the role of the GABAB receptor in the mediation of several alcohol-related behaviors. These data possess remarkable translational value, as most of the above effects of baclofen have ultimately been reproduced in AUD patients.

Multiple timescales of normalized value coding underlie adaptive choice behavior

Adaptation is a fundamental process crucial for the efficient coding of sensory information. Recent evidence suggests that similar coding principles operate in decision-related brain areas, where neural value coding adapts to recent reward history. However, the circuit mechanism for value adaptation is unknown, and the link between changes in adaptive value coding and choice behavior is unclear. Here we show that choice behavior in nonhuman primates varies with the statistics of recent rewards. Consistent with efficient coding theory, decision-making shows increased choice sensitivity in lower variance reward environments. Both the average adaptation effect and across-session variability are explained by a novel multiple timescale dynamical model of value representation implementing divisive normalization. The model predicts empirical variance-driven changes in behavior despite having no explicit knowledge of environmental statistics, suggesting that distributional characteristics can be captured by dynamic model architectures. These findings highlight the importance of treating decision-making as a dynamic process and the role of normalization as a unifying computation for contextual phenomena in choice.

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.

Bridging the gap between rodents and humans: The role of non-human primates in oxytocin research.

Oxytocin (OT), a neuropeptide that acts in the brain as a neuromodulator, has been long known to shape maternal physiology and behavior in mammals, however its role in regulating social cognition and behavior in primates has come to the forefront only in the recent decade. Many of the current perspectives on the role of OT in modulating social behavior emerged first from studies in rodents, where invasive techniques with a high degree of precision have permitted the mechanistic dissection of OT-related behaviors, as well as their underlying neural circuits in exquisite detail. In parallel, behavioral and imaging studies in humans have suggested that brain OT may similarly influence human social behavior and neural activity. These studies in rodents and humans have spurred interest in the therapeutic potential of targeting the OT system to remedy deficits in social cognition and behavior that are present across numerous psychiatric disorders. Yet there remains a tremendous gap in our mechanistic understanding of the influence of brain OT on social neural circuitry between rodents and man. In fact, very little is known regarding the neural mechanisms by which exogenous or endogenous OT influences human social cognition, limiting its therapeutic potential. Here we discuss how non-human primates (NHPs) are uniquely positioned to now bridge the gaps in knowledge provided by the precise circuit-level approaches widely used in rodent models and the behavioral, imaging, and clinical studies in humans. This review provides a perspective on what has been achieved, and what can be expected from exploring the role of OT in shaping social behaviors in NHPs in the coming years.

REVIEW: PSYCHOPATHOLOGIES IN CAPTIVE NONHUMAN PRIMATES AND APPROACHES TO DIAGNOSIS AND TREATMENT.

Despite the growing knowledge and literature on primate medicine, assessment and treatment of behavioral abnormalities in nonhuman primates (NHPs) is an underdeveloped field. There is ample evidence for similarity between humans and great apes, including basic neurologic physiology and emotional processes, and no substantial argument exists against a concept of continuity for abnormal conditions in NHPs that emerge in response to adverse experiences, akin to human psychopathology. NHPs have served as models for human psychopathologies for many decades, but the acquired knowledge has only hesitantly been applied to primates themselves. This review aims to raise awareness among the veterinary community of the wealth of literature on NHP psychopathologies in human medicine and anthropology literature and calls for the necessity to include mental health assessments and professionally structured treatment approaches in NHP medicine. Growing understanding about causes and pathogenesis of abnormal behavior in NHP will not only help to prevent the development of undesirable behaviors but also allow for treatment and management of long-lived, already affected animal patients.

Urinary oxytocin in capuchin monkeys: Validation and the influence of social behavior.

In highly social species, like primates, oxytocin plays an important role in cooperation, and in the formation and maintenance of social relationships. Despite recent interest in the relationship between oxytocin and social behavior in nonhuman primates, relatively little is known about endogenous oxytocin in social New World Monkeys. In this paper, we investigate the relationship between oxytocin and affiliative behaviors in socially-housed captive capuchin monkeys (Sapajus [Cebus] apella) by first validating methods of analysis of urinary oxytocin in this species and, second, examining the effects of grooming and fur-rubbing behavior on oxytocin concentrations and further affiliative behavior. In the validation, we found that intranasal exogenous oxytocin significantly increased urinary oxytocin 15-60 min post-administration. Oxytocin was also implicated in both grooming and fur-rubbing behaviors. We found that oxytocin concentrations increased after subjects engaged in grooming or fur-rubbing. In addition, we found that fur-rubbing influenced affiliative behaviors, both during and after a social fur-rubbing bout. While individuals spent more time in contact and proximity while fur-rubbing, immediately following the fur-rubbing event (15-30 min afterwards) all affiliative behaviors decreased. This supports previous research that oxytocin may, in fact, initially be related to increased social distance in this species. Yet, an increase in all affiliative behaviors 30-45 min after the onset of fur-rubbing suggests that fur-rubbing, like grooming, may ultimately function to strengthen social relationships. Overall, these results support a critical role for oxytocin in affiliative behaviors that maintain and strengthen social relationships in capuchin monkeys, and highlight the complexity of the interactions among oxytocin, affiliative behaviors, and social bonding.

Maternal Diet, Metabolic State, and Inflammatory Response Exert Unique and Long-Lasting Influences on Offspring Behavior in Non-Human Primates.

Nutritional status influences brain health and gestational exposure to metabolic disorders (e.g. obesity and diabetes) increases the risk of neuropsychiatric disorders. The aim of the present study was to further investigate the role of maternal Western-style diet (WSD), metabolic state, and inflammatory factors in the programming of Japanese macaque offspring behavior. Utilizing structural equation modeling, we investigated the relationships between maternal diet, prepregnancy adiposity, third trimester insulin response, and plasma cytokine levels on 11-month-old offspring behavior. Maternal WSD was associated with greater reactive and ritualized anxiety in offspring. Maternal adiposity and third trimester macrophage-derived chemokine (MDC) exerted opposing effects on offspring high-energy outbursts. Elevated levels of this behavior were associated with low maternal MDC and increased prepregnancy adiposity. This is the first study to show that maternal MDC levels influence offspring behavior. We found no evidence suggesting maternal peripheral inflammatory response mediated the effect of maternal diet and metabolic state on aberrant offspring behavior. Additionally, the extent of maternal metabolic impairment differentially influenced chemokine response. Elevated prepregnancy adiposity suppressed third trimester chemokines, while obesity-induced insulin resistance augmented peripheral chemokine levels. WSD also directly increased maternal interleukin-12. This is the first non-human primate study to delineate the effects of maternal diet and metabolic state on gestational inflammatory environment and subsequent offspring behavior. Our findings give insight to the complex mechanisms by which diet, metabolic state, and inflammation during pregnancy exert unique influences on offspring behavioral regulation.

Spermatogonial behavior in marmoset: a new generation, their kinetics and niche.

Could a more detailed evaluation of marmoset spermatogonial morphology, kinetics and niches using high-resolution light microscopy (HRLM) lead to new findings? Three subtypes of marmoset undifferentiated spermatogonia, which were not evenly distributed in terms of number and position along the basal membrane, and an extra premeiotic cell division not present in humans were identified using HRLM. The seminiferous epithelium cycle (SEC) of marmosets is divided into nine stages when based on the acrosome system, and several spermatogenic stages can usually be recognized within the same tubular cross-section. Three spermatogonial generations have been previously described in marmosets: types Adark, Apale and B spermatogonia. Testes from five adult Callithrix penicillata were fixed by glutaraldehyde perfusion via the cardiac route and embedded in Araldite plastic resin for HRLM evaluation. Semi-thin sections (1 μm) were analyzed morphologically and morphometrically to evaluate spermatogonial morphology and kinetics (number, mitosis and apoptosis), spermatogenesis efficiency and the spermatogonial niche. Shape and nuclear diameter, the presence and distribution of heterochromatin, the granularity of the euchromatin, as well as the number, morphology and degree of nucleolar compaction were observed for morphological characterization. Kinetics analyses were performed for all spermatogonial subtypes and preleptotene spermatocytes, and their mitosis and apoptosis indexes determined across all SEC stages. Spermatogenesis parameters (mitotic, meiotic, Sertoli cell workload and general spermatogenesis efficiency) were determined through the counting of Adark and Apale spermatogonia, preleptotene and pachytene primary spermatocytes, round spermatids, and Sertoli cells at stage IV of the SEC. This is the first time that a study in marmosets demonstrates: the existence of a new spermatogonial generation (B2); the presence of two subtypes of Adark spermatogonia with (AdVac) and without (AdNoVac) nuclear rarefaction zones; the peculiar behavior of AdVac spermatogonia across the stages of the SEC, suggesting that they are quiescent stem spermatogonia; and that AdVac spermatogonia are located close to areas in which blood vessels, Leydig cells and macrophages are concentrated, suggesting a niche area for these cells. Not applicable. The C. penicillata spermatogonial kinetics evaluated here consider spermatogonial number across the SEC and their mitotic and apoptotic figures identified in HRLM sections. Therefore, caution is required when comparing absolute values between species. Although morphometric evaluation has suggested that AdVac spermatogonia are stem cells, a functional proof of this is still missing. It is known that parameters of the spermatogenic process in C. penicillata have similarities with those of the common marmoset C. jacchus, however, a detailed study of spermatogonial morphology, kinetics and niche has not yet been performed in C. jacchus, and a full comparison of the two species is not possible. Our findings in C. penicillata contribute to a better understanding of the spermatogonial behavior and spermatogenesis efficiency in non-human primates. Given the phylogenetic closeness of the marmoset to the human species, similar processes might occur in humans. Therefore, marmosets may be an excellent model for studies regarding human testicular biology, fertility and related disorders. Experiments were partially supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) and Conselho Nacional de Desenvolvimento Cientifico e Tecnológico (CNPq). The authors declare that there are no conflicts of interest.

Profile of Dorothy L. Cheney and Robert M. Seyfarth

Field studies in Africa over the past four decades by ethologists Dorothy Cheney and Robert Seyfarth have uncovered a trove of insights into the behavior, communication, and social cognition of nonhuman primates. The pair’s research further reveals evolutionary antecedents of the human mind. University of Pennsylvania professors emeriti, Cheney and Seyfarth are both elected members of the National Academy of Sciences. For her Inaugural Article cowritten with Seyfarth, Cheney strengthens the hypothesis that many primate vocalizations shape social interactions. Factors driving the early stages of language evolution may therefore be associated with primate social challenges. Dorothy Cheney and baboons. Image courtesy of Keena Roberts (photographer). Robert Seyfarth and baboons crossing water. Image courtesy of Dorothy L. Cheney. As youths, Cheney and Seyfarth enjoyed travel and nature. Cheney’s father was in the US Foreign Service, so her family moved to a different place every few years before returning to Washington, DC. “My parents’ rather laissez faire approach to child-rearing allowed my sister and me to travel alone around India in our teenage years,” says Cheney. “We were given complete independence, for which I’ve always been grateful.” Seyfarth’s father was a Chicago-based businessman. “He also loved the outdoors, and on fishing trips to Canada and the Caribbean, taught me how to enjoy the wilderness even when we didn’t catch fish,” Seyfarth says. Cheney and Seyfarth were not initially drawn to science. Cheney preferred history at her preparatory school in Massachusetts, Abbot Academy, and Seyfarth at first struggled with science. He says, “I found science courses difficult and unappealing until, in my senior year at Phillips Exeter Academy in New Hampshire, I took a course on Darwin. The theory of evolution brought everything into focus and made all that memorization seem worthwhile.” Cheney’s “Darwin moment” happened in the spring term of her Wellesley …

Age-related changes in the social behavior of tufted capuchin monkeys.

The effects of aging on the social behavior of nonhuman primates is little understood, especially in New World monkeys. We studied the members of a colony of tufted capuchin monkeys (Sapajus sp.) in order to evaluate age related changes in their social behavior. We conducted observations on 25 subjects aged 4-36 years, living in captive social groups. We found that affiliative interactions (grooming and proximity) decreased with age, and that grooming was increasingly directed to a single preferred partner. Manipulation of objects in the environment also decreased with age, while locomotion and aggression showed no change. Overall, these results concur with previous findings on both human and nonhuman primates, and cast doubts on interpretations of age associated changes in human social behavior that rely of uniquely human advanced cognitive capacities.

Neuromodulation of Prefrontal Cortex in Non-Human Primates by Dopaminergic Receptors during Rule-Guided Flexible Behavior and Cognitive Control.

The prefrontal cortex (PFC) is indispensable for several higher-order cognitive and executive capacities of primates, including representation of salient stimuli in working memory (WM), maintenance of cognitive task set, inhibition of inappropriate responses and rule-guided flexible behavior. PFC networks are subject to robust neuromodulation from ascending catecholaminergic systems. Disruption of these systems in PFC has been implicated in cognitive deficits associated with several neuropsychiatric disorders. Over the past four decades, a considerable body of work has examined the influence of dopamine on macaque PFC activity representing spatial WM. There has also been burgeoning interest in neuromodulation of PFC circuits involved in other cognitive functions of PFC, including representation of rules to guide flexible behavior. Here, we review recent neuropharmacological investigations conducted in our laboratory and others of the role of PFC dopamine receptors in regulating rule-guided behavior in non-human primates. Employing iontophoresis, we examined the effects of local manipulation of dopaminergic subtypes on neuronal activity during performance of rule-guided pro- and antisaccades, an experimental paradigm sensitive to PFC integrity, wherein deficits in performance are reliably observed in many neuropsychiatric disorders. We found dissociable effects of dopamine receptors on neuronal activity for rule representation and oculomotor responses and discuss these findings in the context of prior studies that have examined the role of dopamine in spatial delayed response tasks, attention, target selection, abstract rules, visuomotor learning and reward. The findings we describe here highlight the common features, as well as heterogeneity and context dependence of dopaminergic neuromodulation in regulating the efficacy of cognitive functions of PFC in health and disease.

Avoidance of biological contaminants through sight, smell and touch in chimpanzees.

Avoiding biological contaminants is a well-known manifestation of the adaptive system of disgust. In theory, animals evolved with such a system to prevent pathogen and parasite infection. Bodily products are human-universal disgust elicitors, but whether they also elicit avoidance behaviour in non-human primates has yet to be tested. Here, we report experimental evidence that potential exposure to biological contaminants (faeces, blood, semen), as perceived via multiple sensory modalities (visual, olfactory, tactile), might influence feeding decisions in chimpanzees (Pan troglodytes troglodytes)—our closest phylogenetic relatives. Although somewhat mixed, our results do show increased latencies to feed, tendencies to maintain greater distances from contaminants and/or outright refusals to consume food in test versus control conditions. Overall, these findings are consistent with the parasite avoidance theory of disgust, although the presence of biological contaminants did not preclude feeding entirely. The avoidance behaviours observed hint at the origins of disgust in humans, and further comparative research is now needed.