How chimpanzees look at pictures: a comparative eye-tracking study

Surprisingly little is known about the eye movements of chimpanzees, despite the potential contribution of such knowledge to comparative cognition studies. Here, we present the first examination of eye tracking in chimpanzees. We recorded the eye movements of chimpanzees as they viewed naturalistic pictures containing a full-body image of a chimpanzee, a human or another mammal; results were compared with those from humans. We found a striking similarity in viewing patterns between the two species. Both chimpanzees and humans looked at the animal figures for longer than at the background and at the face region for longer than at other parts of the body. The face region was detected at first sight by both species when they were shown pictures of chimpanzees and of humans. However, the eye movements of chimpanzees also exhibited distinct differences from those of humans; the former shifted the fixation location more quickly and more broadly than the latter. In addition, the average duration of fixation on the face region was shorter in chimpanzees than in humans. Overall, our results clearly demonstrate the eye-movement strategies common to the two primate species and also suggest several notable differences manifested during the observation of pictures of scenes and body forms.     

Clinical outcome of a protocol to produce immunosuppression in rhesus monkeys (Macaca mulatta): application to infectious disease and gene therapy studies

Induced immunosuppression is required for a number of studies using rhesus monkeys (Macaca mulatta). This report describes the clinical outcome and safety of a dose-finding experiment that determined doses of cyclophosphamide and prednisone that could be used to induce a state of immunosuppression in rhesus monkeys. After determining the optimum dose of immunosuppressive agents, the protocol was then used on animals participating in infectious disease and gene therapy studies. Splenectomy was performed in some animals to increase the severity of immunosuppression. The onset, duration, and severity of lymphopenia and leukopenia were consistent in all animals. In most animals, physical examination findings and clinical serum chemistry profiles demonstrated only transient abnormalities. With proper clinical monitoring, combination treatment with cyclophosphamide and prednisone is an effective and safe method for inducing immunosuppression in rhesus monkeys.     

The psychology of primate cooperation and competition: a call for realigning research agendas

Cooperation and competition are two key components of social life. Current research agendas investigating the psychological underpinnings of competition and cooperation in non-human primates are misaligned. The majority of work on competition has been done in the context of theory of mind and deception, while work on cooperation has mostly focused on collaboration and helping. The current impression that theory of mind is not necessarily implicated in cooperative activities and that helping could not be an integral part of competition might therefore be rather misleading. Furthermore, theory of mind research has mainly focused on cognitive aspects like the type of stimuli controlling responses, the nature of representation and how those representations are acquired, while collaboration and helping have focused primarily on motivational aspects like prosociality, common goals and a sense of justice and other-regarding concerns. We present the current state of these two bodies of research paying special attention to how they have developed and diverged over the years. We propose potential directions to realign the research agendas to investigate the psychological underpinnings of cooperation and competition in primates and other animals.     

Experimental evidence for limited vocal recognition in a wild primate: implications for the social complexity hypothesis

Although monitoring social information is a key aspect of the social complexity hypothesis, surprisingly little work has compared social knowledge across different species of wild animals. In the present study, I use playback experiments to test for individual recognition in wild male geladas (Theropithecus gelada) to compare with published accounts of social knowledge in chacma baboons (Papio ursinus). Geladas and baboons are closely related primates living in socially complex groups that differ dramatically in group size—geladas routinely associate with more than 10 times the number of conspecifics than do baboons. Using grunts from non-rival males to simulate approaches, I examined the strength of a subject male''s response when the ‘approach’ was from the direction of (i) non-rival males (control), or (ii) rival males (a more salient stimulus if playback grunts are not recognized by the subject). I compared responses separately based on the degree of social overlap between the caller and the subject. Responses indicate that male geladas, unlike baboons, do not use vocalizations to recognize all of the individuals they regularly encounter. This represents, to my knowledge, the first documented evidence of ‘missing’ social knowledge in a natural primate population. The sharp distinction between baboons and geladas suggests that geladas are either unable or unmotivated to keep track of the individual identity of other males in their multi-level society—even males with whom they have a large degree of social overlap. Thus, these results are consistent with the central assumption of the social complexity hypothesis that social cognition is costly.     

A case report of hepatocellular carcinoma and focal nodular hyperplasia with a myelolipoma in two chimpanzees and a review of spontaneous hepatobiliary tumors in non-human primates

Spontaneous hepatobiliary tumors in non-human primates are uncommon. Here we report a case of hepatic carcinoma and a case of hepatic focal nodular hyperplasia (FNH) and myelolipoma in two captive chimpanzees. A 16-year-old male chimpanzee (4X0392) died after an 8-month history of hepatic amyloidosis and low-grade anemia. Necropsy findings included a hepatic neoplasm with highly pleomorphic hepatocytes arranged into irregular thickened trabeculae. The diagnosis was high-grade hepatocellular carcinoma. A second male chimpanzee (4X0080), 23 years of age, died suddenly of heart failure secondary to cardiomyopathy. An incidental finding at necropsy was a liver mass characterized by multinodularity, prominent fibrous septa, and biliary hyperplasia. These features were consistent with FNH. While 4X0392 had no history of experimental viral exposure, 4X0080 was vaccinated with inactivated hepatitis B virus, an attenuated hepatitis A virus, and was experimentally infected with hepatitis C virus and human immunodeficiency virus. A survey of the literature revealed 68 reported cases of hepatobiliary tumors in non-human primates, including 12 hepatocellular adenomas, eight cholangiocellular adenomas/cystadenomas, 22 hepatocellular carcinomas, seven cholangiocarcinomas, and seven gallbladder adenocarcinomas. The majority of reported cases have been in prosimians and Old World monkeys. Hepatic neoplasia is rare in chimpanzees. Only four hepatic neoplasms have been reported in chimpanzees, three of which were associated with viral hepatitis. FNH has not been previously described in any non-human primate.     

Lethal pneumonia in a captive juvenile chimpanzee (Pan troglodytes) due to human-transmitted human respiratory syncytial virus (HRSV) and infection with Streptococcus pneumoniae

Background  During an outbreak of respiratory disease in captive chimpanzees ( Pan troglodytes ), gorillas ( Gorilla gorilla ), Bornean orangutans ( Pongo pygmaeus ), and red-capped mangabeys ( Cercocebus torquatus ) also staff members showed non-specific upper respiratory signs. One infant female chimpanzee with severe respiratory symptoms died despite immediate medical treatment and was submitted for necropsy.
Methods  Routine post mortem, histological and bacteriological examinations were conducted. Additionally lung tissue samples form the chimpanzee and swab samples from the staff members and the other primates were examined by PCR.
Results  A severe catarrhal to purulent bronchopneumonia and an interstitial pneumonia were found and human respiratory syncytial virus (HRSV) as well as Streptococcus pneumoniae was detected in lung samples by PCR. Swab samples from one animal keeper revealed the same HRSV sequence as of the chimpanzee.
Conclusions  Therefore, it is suggested that the outbreak of respiratory disease within a zoological institution was due to transmission of HRSV between both human and primates.     

Kinetics of stable isotope and body composition in olive baboons (Papio anubis) estimated by deuterium dilution space: a pilot study

Morphometrics and isotope-labelled water were used to determine body composition [total body water, total body fat and fat-free mass (FFM)] of three captive female olive baboons (Papio anubis). Mean mass was 16.5 kg, comparable with other captive settings but heavier than wild olive baboons. Average water content was 66%; FFM averaged 90.5%. Baboon females have less body fat than human counterparts. Compared with captive or wild baboons, these females were adequately nourished for their energy expenditure. A positive association between total mass and FFM existed, but due to the small sample no general relationship was observed for body fat or FFM and condition or size measures. The kinetics of deuterium equilibration in body fluids for baboons was determined as 3-4 hours after injection, similar to that for humans. Deuterium dilution technique appears to be an appropriate method for studying body composition in baboons, although a larger sample is needed for relationships between morphometric indices and body composition.     

Elongation as a factor in artefacts of humans and other animals: an Acheulean example in comparative context

Elongation is a commonly found feature in artefacts made and used by humans and other animals and can be analysed in comparative study. Whether made for use in hand or beak, the artefacts have some common properties of length, breadth, thickness and balance point, and elongation can be studied as a factor relating to construction or use of a long axis. In human artefacts, elongation can be traced through the archaeological record, for example in stone blades of the Upper Palaeolithic (traditionally regarded as more sophisticated than earlier artefacts), and in earlier blades of the Middle Palaeolithic. It is now recognized that elongation extends to earlier Palaeolithic artefacts, being found in the repertoire of both Neanderthals and more archaic humans. Artefacts used by non-human animals, including chimpanzees, capuchin monkeys and New Caledonian crows show selection for diameter and length, and consistent interventions of modification. Both chimpanzees and capuchins trim side branches from stems, and appropriate lengths of stave are selected or cut. In human artefacts, occasional organic finds show elongation back to about 0.5 million years. A record of elongation achieved in stone tools survives to at least 1.75 Ma (million years ago) in the Acheulean tradition. Throughout this tradition, some Acheulean handaxes are highly elongated, usually found with others that are less elongated. Finds from the million-year-old site of Kilombe and Kenya are given as an example. These findings argue that the elongation need not be integral to a design, but that artefacts may be the outcome of adjustments to individual variables. Such individual adjustments are seen in animal artefacts. In the case of a handaxe, the maker must balance the adjustments to achieve a satisfactory outcome in the artefact as a whole. It is argued that the need to make decisions about individual variables within multivariate objects provides an essential continuity across artefacts made by different species.     

Resident bacteria in a mixed population of rhesus macaque (Macaca mulatta) monkeys: a prevalence study

Background  Microflora populations residing in oropharyngeal and gastrointestinal sites defend against pathogenic bacterial colonization. Perturbations in these microbial communities may allow opportunistic pathogenic bacteria to establish themselves and cause morbidity and mortality from sepsis particularly after stressful experimental procedures. This study determined the prevalent facultative bacteria in a resident population of Macaca mulatta prior to use in experimentally induced immunosuppressive radiation studies.
Methods  Standard microbiological methods were used to assess prevalent facultative bacteria in the oropharynx and rectum of 24 male M. mulatta .
Results  The majority of the bacteria isolated from the oropharyngeal and rectal sites were gram-positive cocci. Species of Staphylococcus and Streptococcus predominated in all samples. Few gram-negative bacteria were isolated.
Conclusions  Bacteriological assessment is recommended to identify predominant bacterial species to be prepared to provide appropriate antimicrobial therapy in non-human primates that are expected to undergo stressful immunocompromising procedures.     

Development of a novel xenotransplantation strategy for treatment of diabetes mellitus in rat hosts and translation to non-human primates

Transplantation therapy for diabetes is limited by unavailability of donor organs and outcomes complicated by immunosuppressive drug toxicity. Xenotransplantation is a strategy to overcome supply problems. Implantation of tissue obtained early during embryogenesis is a way to reduce transplant immunogenicity. Insulin-producing cells originating from embryonic pig pancreas obtained very early following pancreatic primordium formation [embryonic day 28 (E28)] engraft long-term in inbred diabetic Lewis or Zucker Diabetic Fatty (ZDF) rats or rhesus macaques. Endocrine cells originating from embryonic pig pancreas transplanted in host mesentery migrate to mesenteric lymph nodes, engraft, normalize glucose tolerance in rats and improve glucose tolerance in rhesus macaques without the need for immune suppression. Engraftment of primordia is permissive for engraftment of an insulin-expressing cell component from porcine islets implanted subsequently without immune suppression. Similarities between findings in inbred rat and non-human primate hosts bode well for successful translation to humans of what could be a novel xenotransplantation strategy for the treatment of diabetes.     

Development of a novel xenotransplantation strategy for treatment of diabetes mellitus in rat hosts and translation to non-human primates

Transplantation therapy for diabetes is limited by unavailability of donor organs and outcomes complicated by immunosuppressive drug toxicity. Xenotransplantation is a strategy to overcome supply problems. Implantation of tissue obtained early during embryogenesis is a way to reduce transplant immunogenicity. Insulin-producing cells originating from embryonic pig pancreas obtained very early following pancreatic primordium formation [embryonic day 28 (E28)] engraft long-term in inbred diabetic Lewis or Zucker Diabetic Fatty (ZDF) rats or rhesus macaques. Endocrine cells originating from embryonic pig pancreas transplanted in host mesentery migrate to mesenteric lymph nodes, engraft, normalize glucose tolerance in rats and improve glucose tolerance in rhesus macaques without the need for immune suppression. Engraftment of primordia is permissive for engraftment of an insulin-expressing cell component from porcine islets implanted subsequently without immune suppression. Similarities between findings in inbred rat and non-human primate hosts bode well for successful translation to humans of what could be a novel xenotransplantation strategy for the treatment of diabetes.     

A word in the hand: action, gesture and mental representation in humans and non-human primates

The movements we make with our hands both reflect our mental processes and help to shape them. Our actions and gestures can affect our mental representations of actions and objects. In this paper, we explore the relationship between action, gesture and thought in both humans and non-human primates and discuss its role in the evolution of language. Human gesture (specifically representational gesture) may provide a unique link between action and mental representation. It is kinaesthetically close to action and is, at the same time, symbolic. Non-human primates use gesture frequently to communicate, and do so flexibly. However, their gestures mainly resemble incomplete actions and lack the representational elements that characterize much of human gesture. Differences in the mirror neuron system provide a potential explanation for non-human primates' lack of representational gestures; the monkey mirror system does not respond to representational gestures, while the human system does. In humans, gesture grounds mental representation in action, but there is no evidence for this link in other primates. We argue that gesture played an important role in the transition to symbolic thought and language in human evolution, following a cognitive leap that allowed gesture to incorporate representational elements.     

Speed and accuracy in nest-mate recognition: a hover wasp prioritizes face recognition over colony odour cues to minimize intrusion by outsiders

Social insects have evolved sophisticated recognition systems enabling them to accept nest-mates but reject alien conspecifics. In the social wasp, Liostenogaster flavolineata (Stenogastrinae), individuals differ in their cuticular hydrocarbon profiles according to colony membership; each female also possesses a unique (visual) facial pattern. This species represents a unique model to understand how vision and olfaction are integrated and the extent to which wasps prioritize one channel over the other to discriminate aliens and nest-mates. Liostenogaster flavolineata females are able to discriminate between alien and nest-mate females using facial patterns or chemical cues in isolation. However, the two sensory modalities are not equally efficient in the discrimination of ‘friend’ from ‘foe’. Visual cues induce an increased number of erroneous attacks on nest-mates (false alarms), but such attacks are quickly aborted and never result in serious injury. Odour cues, presented in isolation, result in an increased number of misses: erroneous acceptances of outsiders. Interestingly, wasps take the relative efficiencies of the two sensory modalities into account when making rapid decisions about colony membership of an individual: chemical profiles are entirely ignored when the visual and chemical stimuli are presented together. Thus, wasps adopt a strategy to ‘err on the safe side’ by memorizing individual faces to recognize colony members, and disregarding odour cues to minimize the risk of intrusion from colony outsiders.     

Nonsocial and social cognition in schizophrenia: current evidence and future directions

Cognitive impairment in schizophrenia involves a broad array of nonsocial and social cognitive domains. It is a core feature of the illness, and one with substantial implications for treatment and prognosis. Our understanding of the causes, consequences and interventions for cognitive impairment in schizophrenia has grown substantially in recent years. Here we review a range of topics, including: a) the types of nonsocial cognitive, social cognitive, and perceptual deficits in schizophrenia; b) how deficits in schizophrenia are similar or different from those in other disorders; c) cognitive impairments in the prodromal period and over the lifespan in schizophrenia; d) neuroimaging of the neural substrates of nonsocial and social cognition, and e) relationships of nonsocial and social cognition to functional outcome. The paper also reviews the considerable efforts that have been directed to improve cognitive impairments in schizophrenia through novel psychopharmacology, cognitive remediation, social cognitive training, and alternative approaches. In the final section, we consider areas that are emerging and have the potential to provide future insights, including the interface of motivation and cognition, the influence of childhood adversity, metacognition, the role of neuroinflammation, computational modelling, the application of remote digital technology, and novel methods to evaluate brain network organization. The study of cognitive impairment has provided a way to approach, examine and comprehend a wide range of features of schizophrenia, and it may ultimately affect how we define and diagnose this complex disorder.     

Differential foraging in presence of predator and conspecific odors in bank voles: a field enclosure study

Bank voles detect and discriminate other organisms, e.g., predators versus conspecifics, based on olfactory clues like urine, feces, or scent marks. The present field enclosure experiment was set up to determine whether scented food is sufficient for inducing such differentiated reactions in bank voles. Fourteen different odors were tested, divided into four categories: (1) terrestrial predators, (2) avian predators, (3) conspecifics, and (4) neutral origin (human, dog, solvent-treated, and unscented). The odors were extracted with methanol from pellets or feces, or were an artificial substitute. To test the influence of odors on the foraging behavior of voles, artificial food patches containing scented feeders were used. The feeders were cleaned and refilled daily with a calibrated amount of food sprayed with 1 ml of a different odor randomly chosen. The patches were also equipped with monochromatic cameras to monitor the occurrences of voles around the feeders. Both the visits at scented feeders and food consumption were analyzed for each odor. The results show that relative to their foraging activity on unscented food, bank voles significantly reduce it on food scented with odors of terrestrial predators, and increase it in the presence of conspecific odors. Their foraging activity was not affected by neutral scent, nor by scents from avian predators. These results prove that bank voles react to scented food in a way that varies according to the source of odor, even in the semi-natural conditions of an outdoor enclosure.     

Plain faces are more expressive: comparative study of facial colour,mobility and musculature in primates

Facial colour patterns and facial expressions are among the most important phenotypic traits that primates use during social interactions. While colour patterns provide information about the sender''s identity, expressions can communicate its behavioural intentions. Extrinsic factors, including social group size, have shaped the evolution of facial coloration and mobility, but intrinsic relationships and trade-offs likely operate in their evolution as well. We hypothesize that complex facial colour patterning could reduce how salient facial expressions appear to a receiver, and thus species with highly expressive faces would have evolved uniformly coloured faces. We test this hypothesis through a phylogenetic comparative study, and explore the underlying morphological factors of facial mobility. Supporting our hypothesis, we find that species with highly expressive faces have plain facial colour patterns. The number of facial muscles does not predict facial mobility; instead, species that are larger and have a larger facial nucleus have more expressive faces. This highlights a potential trade-off between facial mobility and colour patterning in primates and reveals complex relationships between facial features during primate evolution.     

Motor-sensory convergence in object localization: a comparative study in rats and humans

In order to identify basic aspects in the process of tactile perception, we trained rats and humans in similar object localization tasks and compared the strategies used by the two species. We found that rats integrated temporally related sensory inputs ('temporal inputs') from early whisk cycles with spatially related inputs ('spatial inputs') to align their whiskers with the objects; their perceptual reports appeared to be based primarily on this spatial alignment. In a similar manner, human subjects also integrated temporal and spatial inputs, but relied mainly on temporal inputs for object localization. These results suggest that during tactile object localization, an iterative motor-sensory process gradually converges on a stable percept of object location in both species.     

The sound of one-hand clapping: handedness and perisylvian neural correlates of a communicative gesture in chimpanzees

Whether lateralization of communicative signalling in non-human primates might constitute prerequisites of hemispheric specialization for language is unclear. In the present study, we examined (i) hand preference for a communicative gesture (clapping in 94 captive chimpanzees from two research facilities) and (ii) the in vivo magnetic resonance imaging brain scans of 40 of these individuals. The preferred hand for clapping was defined as the one in the upper position when the two hands came together. Using computer manual tracing of regions of interest, we measured the neuroanatomical asymmetries for the homologues of key language areas, including the inferior frontal gyrus (IFG) and planum temporale (PT). When considering the entire sample, there was a predominance of right-handedness for clapping and the distribution of right- and left-handed individuals did not differ between the two facilities. The direction of hand preference (right- versus left-handed subjects) for clapping explained a significant portion of variability in asymmetries of the PT and IFG. The results are consistent with the view that gestural communication in the common ancestor may have been a precursor of language and its cerebral substrates in modern humans.     

Prefrontal cortex in humans and apes: a comparative study of area 10

Area 10 is one of the cortical areas of the frontal lobe involved in higher cognitive functions such as the undertaking of initiatives and the planning of future actions. It is known to form the frontal pole of the macaque and human brain, but its presence and organization in the great and lesser apes remain unclear. It is here documented that area 10 also forms the frontal pole of chimpanzee, bonobo, orangutan, and gibbon brains. Imaging techniques and stereological tools are used to characterize this area across species and provide preliminary estimates of its absolute and relative size. Area 10 has similar cytoarchitectonic features in the hominoid brain, but aspects of its organization vary slightly across species, including the relative width of its cortical layers and the space available for connections. The cortex forming the frontal pole of the gorilla appears highly specialized, while area 10 in the gibbon occupies only the orbital sector of the frontal pole. Area 10 in the human brain is larger relative to the rest of the brain than it is in the apes, and its supragranular layers have more space available for connections with other higher-order association areas. This suggests that the neural substrates supporting cognitive functions associated with this part of the cortex enlarged and became specialized during hominid evolution.