Matching-to-Sample Task Training of a Killer Whale (Orcinus orca).

Matching-to-sample tasks have been a useful method in visual cognitive studies on non-human animals. The use of touch panels in matching-to-sample tasks has contributed to cognitive studies on terrestrial animals; however, there has been a difficulty in using these devices underwater, which is one of the factors that has slowed the progress of visual studies on underwater animals. Cetaceans (e.g., dolphins and whales) are highly adapted to underwater environments, and further studies on their cognitive abilities are needed to advance our understanding of the interactions between environmental factors and the evolution of cognitive abilities. In this study, we aimed to develop a new experimental method in which a captive killer whale performed a matching-to-sample task using a monitor shown through an underwater window as if a touch panel were used. In order to confirm the usefulness of this method, one simple experiment on mirror image discrimination was conducted, and the pairs with mirror images were shown to be more difficult to identify than the pairs with other normal images. The advantages of using this method include (1) simplicity in the devices and stimuli used in the experiments, (2) appropriate and rigorous experimental control, (3) the possibility of increasing the number of individuals to be tested and interspecies comparisons, and (4) contributions to animal welfare. The use of this method solves some of the problems in previous visual cognitive studies on cetaceans, and it suggests the further possibility of future comparative cognitive studies. It is also expected to contribute to animal welfare in terms of cognitive enrichment, and it could help with the proposal of new exhibition methods in zoos and aquariums.

Endodontic Treatment of a Maxillary Incisor Tooth in a Chimpanzee (Pan troglodytes).

Chimpanzees (Pan troglodytes) with teeth severely damaged by dental caries and/or periodontal disease are often managed with medication and/or tooth extraction. A common endodontic treatment for severely decayed teeth in a 26-year-old female chimpanzee is reported. The left maxillary central incisor tooth had lost its crown, probably due to trauma that was not recent, and it had a fistula most likely due to chronic apical periodontitis. The diagnosis was confirmed radiographically before treatment. To treat the infected root canal, endodontic treatment used in humans was adapted for a chimpanzee. After the treatment, the tooth was sealed using an adhesive resin composite. At 11-years post-treatment, there were no signs of recurrence of the lesion or of failure of the tooth seal. The results of this case report suggest that common endodontic treatments used in humans are also effective in chimpanzees.

Fearful snake pictures make monkeys pessimistic.

Judgment bias is the cognitive tendency of animals experiencing negative (or positive) affect to expect undesirable (or favorable) outcomes in ambiguous situations. The lack of examination of judgment biases induced by ecologically relevant stimuli hampers our understanding of the adaptive role of these biases. We examined whether predator-related stimuli, i.e., pictures of snakes, induce a pessimistic judgment bias in Japanese macaques (Macaca fuscata). Our subjects underwent a touchscreen-based Go/No-go judgment bias test. We found that the subjects were less likely and slower to make Go responses to ambiguous stimuli after viewing the snake pictures, indicating that pictures of snakes induce a pessimistic evaluation of ambiguous stimuli. In environments with high levels of threat, behavioral strategies that reduce risk-taking would be evolutionarily advantageous. Hence, an affective response system that lowers expectations of favorable outcomes in ambiguous situations after encountering threat-related stimuli would serve adaptive purposes, such as curbing excessive exploratory behavior.

Staring death in the face: chimpanzees' attention towards conspecific skulls and the implications of a face module guiding their behaviour.

Chimpanzees exhibit a variety of behaviours surrounding their dead, although much less is known about how they respond towards conspecific skeletons. We tested chimpanzees' visual attention to images of conspecific and non-conspecific stimuli (cat/chimp/dog/rat), shown simultaneously in four corners of a screen in distinct orientations (frontal/diagonal/lateral) of either one of three types (faces/skulls/skull-shaped stones). Additionally, we compared their visual attention towards chimpanzee-only stimuli (faces/skulls/skull-shaped stones). Lastly, we tested their attention towards specific regions of chimpanzee skulls. We theorized that chimpanzee skulls retaining face-like features would be perceived similarly to chimpanzee faces and thus be subjected to similar biases. Overall, supporting our hypotheses, the chimpanzees preferred conspecific-related stimuli. The results showed that chimpanzees attended: (i) significantly longer towards conspecific skulls than other species skulls (particularly in forward-facing and to a lesser extent diagonal orientations); (ii) significantly longer towards conspecific faces than other species faces at forward-facing and diagonal orientations; (iii) longer towards chimpanzee faces compared with chimpanzee skulls and skull-shaped stones, and (iv) attended significantly longer to the teeth, similar to findings for elephants. We suggest that chimpanzee skulls retain relevant, face-like features that arguably activate a domain-specific face module in chimpanzees' brains, guiding their attention.

Chimpanzees (Pan troglodytes) detect strange body parts: an eye-tracking study.

This study investigated chimpanzee body representation by testing whether chimpanzees detect strangeness in body parts. We tested six chimpanzees with edited chimpanzee body pictures in eye-tracking tasks. The target body parts were arms or legs. For either target, there were four conditions: "normal" condition as control, where all bodies were normal; "misplaced" condition, where one arm or one leg was misplaced to an incorrect body location in each picture; "replaced by a chimpanzee part" condition, where one arm or one leg was replaced by a chimpanzee leg or arm, respectively, in its original place in each picture; and "replaced by a human part" condition, where one arm or one leg was replaced by a human arm or leg in each picture. Compared to the looking times toward the normal parts, chimpanzees had significantly longer looking times toward the human arms or legs. The looking times toward the misplaced parts were also longer than the normal parts, but the difference just failed to meet significance. These results indicate more interests toward strange body parts, compared to typical parts, suggesting that chimpanzees might have a body representation that is sufficiently sensitive to detect these aspects of strangeness.

No evidence of spatial representation of age, but "own-age bias" like face processing found in chimpanzees.

Previous studies have revealed that non-human primates can differentiate the age category of faces. However, the knowledge about age recognition in non-human primates is very limited and whether non-human primates can process facial age information in a similar way to humans is unknown. As humans have an association between time and space (e.g., a person in an earlier life stage to the left and a person in a later life stage to the right), we investigated whether chimpanzees spatially represent conspecifics' adult and infant faces. Chimpanzees were tested using an identical matching-to-sample task with conspecific adult and infant face stimuli. Two comparison images were presented vertically (Experiment 1) or horizontally (Experiment 2). We analyzed whether the response time was influenced by the position and age category of the target stimuli, but there was no evidence of correspondence between space and adult/infant faces. Thus, evidence of the spatial representation of the age category was not found. However, we did find that the response time was consistently faster when they discriminated between adult faces than when they discriminated between infant faces in both experiments. This result is in line with a series of human face studies that suggest the existence of an "own-age bias." As far as we know, this is the first report of asymmetric face processing efficiency between infant and adult faces in non-human primates.

Impairment effect of infantile coloration on face discrimination in chimpanzees.

Impaired face recognition for certain face categories, such as faces of other species or other age class faces, is known in both humans and non-human primates. A previous study found that it is more difficult for chimpanzees to differentiate infant faces than adult faces. Infant faces of chimpanzees differ from adult faces in shape and colour, but the latter is especially a salient cue for chimpanzees. Therefore, impaired face differentiation of infant faces may be due to a specific colour. In the present study, we investigated which feature of infant faces has a greater effect on face identification difficulty. Adult chimpanzees were tested using a matching-to-sample task with four types of face stimuli whose shape and colour were manipulated as either infant or adult one independently. Chimpanzees' discrimination performance decreased as they matched faces with infant coloration, regardless of the shape. This study is the first to demonstrate the impairment effect of infantile coloration on face recognition in non-human primates, suggesting that the face recognition strategies of humans and chimpanzees overlap as both species show proficient face recognition for certain face colours.

Spontaneous categorization of tools based on observation in children and chimpanzees.

The acquisition of the concept of 'tool' remains intriguing from both developmental and comparative perspectives. Our current model of tool use development in children is based on humans' supposedly unique ability to adopt a teleological stance: the understanding of a demonstrator's goal-based intentions when using a tool. It is however unclear how children and chimpanzees, our closest relatives, combine their knowledge of different objects whose function is to act on other parts of the environment, and assign them to a single category of 'tools'. Here, we used a function-based approach to address this question. We exposed 7 to 11-year-old children and adult chimpanzees to a Matching-to-Function (MTF) task to explore whether they would sort tools and non-tools separately after demonstration of their function by an experimenter. MTF is a variant of Matching-to-Sample where the sample and the target are from the same category/kind rather than identical. Around 40% of children paired objects according to their function in the MTF task, with only one child younger than 8 years doing so. Moreover, when verbally questioned, these children offered a function-based answer to explain their choices. One of six chimpanzees also successfully paired objects according to function. Children and at least one chimpanzee can thus spontaneously sort tools into functional categories based on observing a demonstrator. The success of a single chimpanzee in our task suggests that teleological reasoning might already have been present in our last common ancestor but also shows that human children more readily conceptualize tools in a spontaneous fashion.

Touch-screen-guided task reveals a prosocial choice tendency by chimpanzees (Pan troglodytes).

Humans help others even without direct benefit for themselves. However, the nature of altruistic (i.e., only the other benefits) and prosocial (i.e., self and other both benefit) behaviors in our closest living relative, the chimpanzee, remains controversial. To address this further, we developed a touch-screen-guided task that allowed us to increase the number of trials for a thorough test of chimpanzees' prosocial and altruistic tendencies. Mother-offspring dyads were tested in the same compartment; one was the actor while the other was the recipient. In Experiment 1, the actor chose among three options: prosocial, selfish (only the actor benefited) and altruistic. To better understand the nature of the chimpanzees' choices and to improve experimental control, we conducted two additional experiments. Experiment 2 consisted of two-option choices interspersed with three-option choices, and in Experiment 3 the two-option choice were blocked across all trials. The results of Experiment 1 clearly showed that chimpanzees acted prosocially in the touch-screen-guided task, choosing the prosocial option on an average of 79% of choices. Five out of the six chimpanzees showed the preference to act prosocially against chance level. The preference for the prosocial option persisted when conditions were changed in Experiments 2 and 3. When only selfish and altruistic options were available in Experiments 2 and 3, chimpanzees preferred the selfish option. These results suggest that (1) most individuals understood the nature of the task and modified their behavior according to the available options, (2) five out of the six chimpanzees chose to act prosocially when they had the option to, and (3) offspring counterbalanced between altruistic and selfish, when given those two options perhaps to avoid suffering repercussions from the mother.

Spontaneous spatial mapping of learned sequence in chimpanzees: evidence for a SNARC-like effect.

In the last couple of decades, there has been a growing number of reports on space-based representation of numbers and serial order in humans. In the present study, to explore evolutionary origins of such representations, we examined whether our closest evolutionary relatives, chimpanzees, map an acquired sequence onto space in a similar way to humans. The subjects had been trained to perform a number sequence task in which they touched a sequence of "small" to "large" Arabic numerals presented in random locations on the monitor. This task was presented in sessions that also included test trials consisting of only two numerals (1 and 9) horizontally arranged. On half of the trials 1 was located to the left of 9, whereas on the other half 1 was to the right to 9. The Chimpanzees' performance was systematically influenced by the spatial arrangement of the stimuli; specifically, they responded quicker when 1 was on the left and 9 on the right compared to the other way around. This result suggests that chimpanzees, like humans, spontaneously map a learned sequence onto space.

Conceptual metaphorical mapping in chimpanzees (Pan troglodytes).

Conceptual metaphors are linguistic constructions. Such a metaphor is humans' mental representation of social rank as a pyramidal-like structure. High-ranked individuals are represented in higher positions than low-ranked individuals. We show that conceptual metaphorical mapping between social rank and the representational domain exists in our closest evolutionary relatives, the chimpanzees. Chimpanzee participants were requested to discriminate face identities in a vertical arrangement. We found a modulation of response latencies by the rank of the presented individual and the position on the display: a high-ranked individual presented in the higher and a low-ranked individual in the lower position led to quicker identity discrimination than a high-ranked individual in the lower and a low-ranked individual in the higher position. Such a spatial representation of dominance hierarchy in chimpanzees suggests that a natural tendency to systematically map an abstract dimension exists in the common ancestor of humans and chimpanzees. DOI:http://dx.doi.org/10.7554/eLife.00932.001.

Laterality effect for faces in chimpanzees (Pan troglodytes).

Face perception in humans is governed more by right-hemispheric than left-hemispheric neural correlate. Some but not all neurophysiological studies depict a right-side dominance for face responsive neurons in the brains of macaques. Hence, it is an open question whether and to what extent a right-hemisphere preference of processing faces exists across primate brains. We investigated chimpanzees discriminating chimeric faces of chimpanzees and humans, i.e., the combination of either left or right sides of a face vertically flipped and merged into a whole face. We found an effect of choosing the left-chimeric face more often than the right-chimeric face as being the one of the two that is closer to the original face, reflecting an advantage for the right side of the brain to process faces, as reported in humans. Moreover, we found a modulation by age of the participants, suggesting that the exposure history with a particular category shapes the right-hemispheric neural correlate to a configural/holistic processing strategy. In other words, the findings in chimpanzee participants parallel those in human participants and are suggestive for similar neural machineries in the occipital-temporal cortices in both species.

The face inversion effect in non-human primates revisited - an investigation in chimpanzees (Pan troglodytes).

Faces presented upside-down are harder to recognize than presented right-side up, an effect known as the face inversion effect. With inversion the perceptual processing of the spatial relationship among facial parts is disrupted. Previous literature indicates a face inversion effect in chimpanzees toward familiar and conspecific faces. Although these results are not inconsistent with findings from humans they have some controversy in their methodology. Here, we employed a delayed matching-to-sample task to test captive chimpanzees on discriminating chimpanzee and human faces. Their performances were deteriorated by inversion. More importantly, the discrimination deterioration was systematically different between the two age groups of chimpanzee participants, i.e. young chimpanzees showed a stronger inversion effect for chimpanzee than for human faces, while old chimpanzees showed a stronger inversion effect for human than for chimpanzee faces. We conclude that the face inversion effect in chimpanzees is modulated by the level of expertise of face processing.

Perception of the motion trajectory of objects from moving cast shadows in infant Japanese macaques (Macaca fuscata).

The shadows cast by moving objects enable human adults and infants to infer the motion trajectories of objects. Nonhuman animals must also be able to discriminate between objects and their shadows and infer the spatial layout of objects from cast shadows. However, the evolutionary and comparative developmental origins of sensitivity to cast shadows have not been investigated. In this study, we used a familiarity/novelty preferential looking procedure to assess the ability of infant macaques, aged 7-24 weeks, to discriminate between a 'depth' display containing a ball and cast shadow moving diagonally and an 'up' display containing a ball with a diagonal trajectory and a shadow with a horizontal trajectory. The infant macaques could discriminate the trajectories of the balls based on the moving shadows. These findings suggest that the ability to perceive the motion trajectory of an object from the moving shadow is common to both humans and macaques.

Developmental processes in face perception.

Understanding the developmental origins of face recognition has been the goal of many studies of various approaches. Contributions of experience-expectant mechanisms (early component), like perceptual narrowing, and lifetime experience (late component) to face processing remain elusive. By investigating captive chimpanzees of varying age, a rare case of a species with lifelong exposure to non-conspecific faces at distinctive levels of experience, we can disentangle developmental components in face recognition. We found an advantage in discriminating chimpanzee above human faces in young chimpanzees, reflecting a predominant contribution of an early component that drives the perceptual system towards the conspecific morphology, and an advantage for human above chimpanzee faces in old chimpanzees, reflecting a predominant late component that shapes the perceptual system along the critical dimensions of the face exposed to. We simulate the contribution of early and late components using computational modeling and mathematically describe the underlying functions.

Visuoauditory mappings between high luminance and high pitch are shared by chimpanzees (Pan troglodytes) and humans.

Humans share implicit preferences for certain cross-sensory combinations; for example, they consistently associate higher-pitched sounds with lighter colors, smaller size, and spikier shapes. In the condition of synesthesia, people may experience such cross-modal correspondences to a perceptual degree (e.g., literally seeing sounds). So far, no study has addressed the question whether nonhuman animals share cross-modal correspondences as well. To establish the evolutionary origins of cross-modal mappings, we tested whether chimpanzees (Pan troglodytes) also associate higher pitch with higher luminance. Thirty-three humans and six chimpanzees were required to classify black and white squares according to their color while hearing irrelevant background sounds that were either high-pitched or low-pitched. Both species performed better when the background sound was congruent (high-pitched for white, low-pitched for black) than when it was incongruent (low-pitched for white, high-pitched for black). An inherent tendency to pair high pitch with high luminance hence evolved before the human lineage split from that of chimpanzees. Rather than being a culturally learned or a linguistic phenomenon, this mapping constitutes a basic feature of the primate sensory system.

Rhesus monkeys see who they hear: spontaneous cross-modal memory for familiar conspecifics.

Rhesus monkeys gather much of their knowledge of the social world through visual input and may preferentially represent this knowledge in the visual modality. Recognition of familiar faces is clearly advantageous, and the flexibility and utility of primate social memory would be greatly enhanced if visual memories could be accessed cross-modally either by visual or auditory stimulation. Such cross-modal access to visual memory would facilitate flexible retrieval of the knowledge necessary for adaptive social behavior. We tested whether rhesus monkeys have cross-modal access to visual memory for familiar conspecifics using a delayed matching-to-sample procedure. Monkeys learned visual matching of video clips of familiar individuals to photographs of those individuals, and generalized performance to novel videos. In crossmodal probe trials, coo-calls were played during the memory interval. The calls were either from the monkey just seen in the sample video clip or from a different familiar monkey. Even though the monkeys were trained exclusively in visual matching, the calls influenced choice by causing an increase in the proportion of errors to the picture of the monkey whose voice was heard on incongruent trials. This result demonstrates spontaneous cross-modal recognition. It also shows that viewing videos of familiar monkeys activates naturally formed memories of real monkeys, validating the use of video stimuli in studies of social cognition in monkeys.

Reverse-reward learning in squirrel monkeys (Saimiri sciureus): retesting after 5 years, and assessment on qualitative transfer.

Seven squirrel monkeys (Saimiri sciureus) previously trained on reverse-reward tasks were presented with the original "1-versus-4" task after a 5-year interval without reverse-reward experience (Experiment 1). None of them reliably selected the smaller food array; however, at around chance level, their performance was superior to when they were first exposed to the task almost 6 years previously, suggesting some long-term memory retention. One naive monkey consistently selected the larger array, as expected. In Experiment 2, trials consisting of 1 versus 1 piece of two qualitatively different types of food were interspersed among familiar 1-versus-4 trials. None of five monkeys tested reliably selected the less-preferred food to get the more preferred food as the reward, and one monkey scored below chance. However, when one piece of low-preference food was paired with four pieces of high-preference food (Experiment 3), all four monkeys tested avoided reaching for the latter and thereby obtained it as the reward; two monkeys obtained perfect scores on these trials. These two monkeys were trained on a specific qualitative reverse-reward pairing and then again tested on new pairings (Experiment 4), but transfer was incomplete. Compound trials that pit quantity against quality in novel ways appear taxing for squirrel monkeys, despite competence in reverse-reward on both dimensions separately.

Rhesus monkeys (Macaca mulatta) rapidly learn to select dominant individuals in videos of artificial social interactions between unfamiliar conspecifics.

Social animals, such as primates, must behave appropriately in complex social situations such as dominance interactions. Learning dominance information through trial and error would be dangerous; therefore, cognitive mechanisms for rapid learning of dominance information by observation would be adaptive. We used a set of digitally edited artificial social interactions to examine whether rhesus monkeys (Macaca mulatta) can learn dominance relationships between unfamiliar conspecifics through observation. Our method allowed random assignment of stimulus monkeys to ranks in an artificial hierarchy, controlling for nonbehavioral cues that could indicate dominance. Subject monkeys watched videos depicting 1 stimulus monkey behaving dominantly toward another and were rewarded for selecting the dominant individual. Monkeys rapidly learned this discrimination across 5 behavior types in Experiment 1 and transferred performance to novel videos of new individuals in Experiment 2. In addition, subjects selected the dominant individual more often than expected by chance in probe videos containing no behavioral dominance information, indicating some retention of the relative dominance status of stimulus monkeys from training. Together, our results suggest that monkeys can learn dominance hierarchies through observation of third-party social interactions.

Asymmetric perception of radial expansion/contraction in Japanese macaque (Macaca fuscata) infants.

Visual radial expansion/contraction motion provides important visual information that is used to control several adaptive actions. We investigated radial motion perception in infant Japanese macaque monkeys using an experimental procedure previously developed for human infants. We found that the infant monkeys' visual preference for the radial expansion pattern was greater than that for the radial contraction pattern. This trend towards an "expansion bias" is similar to that observed in human infants. These results suggest that asymmetrical radial motion processing is a basic visual function common to primates, and that it emerges early in life.