Group-living typically provides benefits to individual group members but also confers costs. To avoid incredulity and betrayal and allow trust and cooperation, individuals must understand the intentions and emotions of their group members. Humans attend to other's eyes and from gaze and pupil-size cues, infer information about the state of mind of the observed. In humans, pupil-size tends to mimic that of the observed. Here we tested whether pupil-mimicry exists in our closest relative, the chimpanzee (P. troglodytes). We conjectured that if pupil-mimicry has adaptive value, e.g. to promote swift communication of inner states and facilitate shared understanding and coordination, pupil-mimicry should emerge within but not across species. Pupillometry data was collected from human and chimpanzee subjects while they observed images of the eyes of both species with dilating/constricting pupils. Both species showed enhanced pupil-mimicry with members of their own species, with effects being strongest in humans and chimpanzee mothers. Pupil-mimicry may be deeply-rooted, but probably gained importance from the point in human evolution where the morphology of our eyes became more prominent. Humans' white sclera surrounding the iris, and the fine muscles around their eyes facilitate non-verbal communication via eye signals.
In April 2009, a female chimpanzee named Sango, living in a captive group at the Noichi Zoo, Japan, gave birth to dizygotic male-female twin chimpanzees (male: Daiya, female: Sakura). The extent to which adult group members cared for the twins was investigated using a focal animal sampling method targeting six adults (one male) when the twin chimpanzees were two years old. Data were collected for an average of 6.78?h (SD = 0.79) per focal participant. An unaffiliated female adult of Sango was engaged in parenting Sakura as much as Sango. Given that Sakura was in lesser proximity to Sango than Daiya, Sakura's departures from her mother and her ability to gesture requests might have enabled non-kin adults to provide her care.
Despite evidence supporting an early attraction to human faces, the nature of the face representation in neonates and its development during the first year after birth remain poorly understood. One suggestion is that an early preference for human faces reflects an attraction toward human eyes because human eyes are distinctive compared with other animals. In accord with this proposal, prior empirical studies have demonstrated the importance of the eye region in face processing in adults and infants. However, an attraction for the human eye has never been shown directly in infants. The current study aimed to investigate whether an attraction for human eyes would be present in newborns and older infants. With the use of a preferential looking time paradigm, newborns and 3-, 6-, 9-, and 12-month-olds were simultaneously presented with a pair of nonhuman primate faces (chimpanzees and Barbary macaques) that differed only by the eyes, thereby pairing a face with original nonhuman primate eyes with the same face in which the eyes were replaced by human eyes. Our results revealed that no preference was observed in newborns, but a preference for nonhuman primate faces with human eyes emerged from 3months of age and remained stable thereafter. The findings are discussed in terms of how a preference for human eyes may emerge during the first few months after birth.
Humans are often unaware of how they control their limb motor movements. People pay attention to their own motor movements only when their usual motor routines encounter errors. Yet little is known about the extent to which voluntary actions rely on automatic control and when automatic control shifts to deliberate control in nonhuman primates. In this study, we demonstrate that chimpanzees and humans showed similar limb motor adjustment in response to feedback error during reaching actions, whereas attentional allocation inferred from gaze behavior differed. We found that humans shifted attention to their own motor kinematics as errors were induced in motor trajectory feedback regardless of whether the errors actually disrupted their reaching their action goals. In contrast, chimpanzees shifted attention to motor execution only when errors actually interfered with their achieving a planned action goal. These results indicate that the species differed in their criteria for shifting from automatic to deliberate control of motor actions. It is widely accepted that sophisticated motor repertoires have evolved in humans. Our results suggest that the deliberate monitoring of one's own motor kinematics may have evolved in the human lineage.
Bottlenose dolphins use auditory (or echoic) information to recognise their environments, and many studies have described their echolocation perception abilities. However, relatively few systematic studies have examined their visual perception. We tested dolphins on a visual-matching task using two-dimensional geometric forms including various features. Based on error patterns, we used multidimensional scaling to analyse perceptual similarities among stimuli. In addition to dolphins, we conducted comparable tests with terrestrial species: chimpanzees were tested on a computer-controlled matching task and humans were tested on a rating task. The overall perceptual similarities among stimuli in dolphins were similar to those in the two species of primates. These results clearly indicate that the visual world is perceived similarly by the three species of mammals, even though each has adapted to a different environment and has differing degrees of dependence on vision.
Many recent comparative studies have addressed "episodic" memory in nonhuman animals, suggesting that birds, rodents, great apes, and others can remember their own behavior after at least a half-day delay. By contrast, despite numerous studies regarding long-term memory, few comparable studies have been conducted on short-term retention for own behavior. In the current study, we addressed the following question: Do chimpanzees remember what they have just done? Four chimpanzees performed matching-to-sample and visual search tasks on a routine basis and were occasionally (every four sessions) given a "recognition" test immediately after their response during visual search trials. Even though these test trials were given very rarely, all four chimpanzees chose the stimulus they selected in the visual search trials immediately before the test trial significantly more frequently than they chose the stimulus they selected in another distractor trial. Subsequent experiments ruled out the possibility that preferences for the specific stimuli accounted for the recognition test results. Thus, chimpanzees remembered their own behavior even within a short-term interval. This type of memory may involve the transfer of episodic information from working memory to long-term episodic-like memory (i.e., an episodic buffer).
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.
An intracranial arachnoid cyst was detected in a 32-year-old, 44.6-kg, female chimpanzee at the Primate Research Institute, Kyoto University. Magnetic resonance imaging (MRI) and computed tomography (CT) were performed and the cognitive studies in which she participated were reviewed. MRI revealed that the cyst was present in the chimpanzees right occipital convexity, and was located in close proximity to the posterior horn of the right lateral ventricle without ventriculomegaly. CT confirmed the presence of the cyst and no apparent signs indicating previous skull fractures were found. The thickness of the mandible was asymmetrical, whereas the temporomandibular joints and dentition were symmetrical. She showed no abnormalities in various cognitive studies since she was 3 years old, except a different behavioural pattern during a recent study, indicating a possible visual field defect. Detailed cognitive studies, long-term observation of her physical condition and follow-up MRI will be continued.
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.
Humans have a superior ability to integrate spatially separate visual information into an entire image. In contrast, comparative cognitive studies have demonstrated that nonhuman primates and avian species are superior in processing relatively local features; however, animals in these studies were required to ignore local shape when they perceived the global configuration, and no studies have directly examined the ability to integrate temporally separate events. In this study, we compared the spatio-temporal visual integration of chimpanzees and humans by exploring dynamic shape perception under a slit-viewing condition. The findings suggest that humans exhibit greater temporal integration accuracy than do chimpanzees. The results show that the ability to integrate local visual information into a global whole is among the unique characteristics of humans.
Deficits in the occipital cortex have varying consequences among mammalian species. Such variations are indicative of evolutionary transitions in the striate cortical contribution to visually guided behavior. However, little is known about the role of the striate cortex in visually guided behavior in chimpanzees due to ethical concerns about invasive experiments and methodological limitations such as the inability to monitor gaze movements. We had the opportunity to study the behavioral consequences of a deficit in the occipital cortex in a chimpanzee with a naturally occurring arachnoid cyst in her right occipital lobe. We assessed the chimpanzees ability to detect a small light probe (0.5 visual degree, Michelson contrast > 0.9) presented at several locations in the visual field while monitoring gaze direction using an infra-red remote eye-tracker recently introduced to studies of great apes. The results showed the chimpanzee was unable to detect the probe in the lower left quadrant of the visual field, suggesting severe loss of contrast sensitivity in a part of hemivisual field that is retinotopically corresponded to the hemisphere of the cyst. A chimpanzee with a naturally occurring deficit in the right striate cortex and the availability of remote eye-tracking technology presented a unique opportunity to compare the role of the occipital lobe in visually guided behavior among various primate species.
Humans actively use behavioral synchrony such as dancing and singing when they intend to make affiliative relationships. Such advanced synchronous movement occurs even unconsciously when we hear rhythmically complex music. A foundation for this tendency may be an evolutionary adaptation for group living but evolutionary origins of human synchronous activity is unclear. Here we show the first evidence that a member of our closest living relatives, a chimpanzee, spontaneously synchronizes her movement with an auditory rhythm: After a training to tap illuminated keys on an electric keyboard, one chimpanzee spontaneously aligned her tapping with the sound when she heard an isochronous distractor sound. This result indicates that sensitivity to, and tendency toward synchronous movement with an auditory rhythm exist in chimpanzees, although humans may have expanded it to unique forms of auditory and visual communication during the course of human evolution.
Ground surfaces play an important role in terrestrial species locomotion and ability to manipulate objects. In humans, ground surfaces have been found to offer significant advantages in distance perception and visual-search tasks ("ground dominance"). The present study used a comparative perspective to investigate the ground-dominance effect in chimpanzees, a species that spends time both on the ground and in trees. During the experiments chimpanzees and humans engaged in a search for a cube on a computer screen; the target cube was darker than other cubes. The search items were arranged on a ground-like or ceiling-like surface, which was defined by texture gradients and shading. The findings indicate that a ground-like, but not a ceiling-like, surface facilitated the search for a difference in luminance among both chimpanzees and humans. Our findings suggest the operation of a ground-dominance effect on visual search in both species.
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.
This study offers a new method for examining the bodily, manual, and eye movements of a chimpanzee at the micro-level. A female chimpanzee wore a lightweight head-mounted eye tracker (60 Hz) on her head while engaging in daily interactions with the human experimenter. The eye tracker recorded her eye movements accurately while the chimpanzee freely moved her head, hands, and body. Three video cameras recorded the bodily and manual movements of the chimpanzee from multiple angles. We examined how the chimpanzee viewed the experimenter in this interactive setting and how the eye movements were related to the ongoing interactive contexts and actions. We prepared two experimentally defined contexts in each session: a face-to-face greeting phase upon the appearance of the experimenter in the experimental room, and a subsequent face-to-face task phase that included manual gestures and fruit rewards. Overall, the general viewing pattern of the chimpanzee, measured in terms of duration of individual fixations, length of individual saccades, and total viewing duration of the experimenters face/body, was very similar to that observed in previous eye-tracking studies that used non-interactive situations, despite the differences in the experimental settings. However, the chimpanzee viewed the experimenter and the scene objects differently depending on the ongoing context and actions. The chimpanzee viewed the experimenters face and body during the greeting phase, but viewed the experimenters face and hands as well as the fruit reward during the task phase. These differences can be explained by the differential bodily/manual actions produced by the chimpanzee and the experimenter during each experimental phase (i.e., greeting gestures, task cueing). Additionally, the chimpanzees viewing pattern varied depending on the identity of the experimenter (i.e., the chimpanzees prior experience with the experimenter). These methods and results offer new possibilities for examining the natural gaze behavior of chimpanzees.
Advancement of non-invasive brain imaging techniques has allowed us to examine details of neural activities involved in affective processing in humans; however, no comparative data are available for chimpanzees, the closest living relatives of humans. In the present study, we measured event-related brain potentials in a fully awake adult chimpanzee as she looked at affective and neutral pictures. The results revealed a differential brain potential appearing 210 ms after presentation of an affective picture, a pattern similar to that in humans. This suggests that at least a part of the affective process is similar between humans and chimpanzees. The results have implications for the evolutionary foundations of emotional phenomena, such as emotional contagion and empathy.
The aim of this study was to analyze the distribution and phenotypic properties of the indigenous streptococci in chimpanzee (Pan troglodytes) oral cavities. Eleven chimpanzees (aged from 9 to 44 years, mean?±?SD, 26.9?±?12.6 years) in the Primate Research Institute of Kyoto University were enrolled in this research and brushing bacterial samples collected from them. Streptococci were isolated from the oral cavities of all chimpanzees. The isolates (n?=?46) were identified as thirteen species by 16S rRNA genes analysis. The predominant species was Streptococcus sanguinis of mitis streptococci from five chimpanzees (45%). Mutans streptococci were isolated from six chimpanzees (55%). The predominant species in the mutans streptococci were Streptococcus troglodytae from four chimpanzees (36%), this species having been proposed as a novel species by us, and Streptococcus dentirousetti from three chimpanzees (27%). Streptococcus mutans was isolated from one chimpanzee (9%). However, Streptococcus sobrinus, Streptococcus macacae and Streptococcus downei, which are indigenous to human and monkey (Macaca fasciclaris) oral habitats, were not isolated. Of the mutans streptococci, S. troglodytae, S. dentirousetti, and S. mutans possessed strong adherence activity to glass surface.
Aim of this study was to analyze the distribution and the phenotypic properties of the indigenous streptococci in the chimpanzee (Pan troglodytes) oral cavities. Eleven chimpanzees (from 9 to 44, average?±?SD, 26.9?±?12.6 years old) in the primate research institutes, Kyoto University, were enrolled in this research, and their brushing bacterial samples were collected. As the results, streptococci were isolated from the oral cavities of all chimpanzees. The isolates (n?=?46) were identified as thirteen species by the 16S rRNA genes analysis. The predominant species was Streptococcus sanguinis of the mitis streptococci from five chimpanzees (45%). The mutans streptococci were isolated from six chimpanzees (55%). The predominant species in the mutans streptococci were Streptococcus troglodytae from four chimpanzees (36%), which species had been proposed as a novel species by us, and Streptococcus dentirousetti from three chimpanzees (27%). Streptococcus mutans, was isolated from one chimpanzee (9%), however, Streptococcus sobrinus, Streptococcus macacae and Streptococcus downei, which are indigenous human or monkey (Macaca fasciclaris) oral habitats, were not isolated. S. troglodytae, S. dentirousetti, and S. mutans of the mutans streptococci possessed strong adherence activity to glass surface.
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.
The present study was performed to investigate the associations between eye-blink behaviors and various other factors in primates. We video-recorded 141 individuals across 71 primate species and analyzed the blink rate, blink duration, and "isolated" blink ratio (i.e., blinks without eye or head movement) in relation to activity rhythms, habitat types, group size, and body size factors. The results showed close relationships between three types of eye-blink measures and body size factors. All of these measures increased as a function of body weight. In addition, diurnal primates showed more blinks than nocturnal species even after controlling for body size factors. The most important findings were the relationships between eye-blink behaviors and social factors, e.g., group size. Among diurnal primates, only the blink rate was significantly correlated even after controlling for body size factors. The blink rate increased as the group size increased. Enlargement of the neocortex is strongly correlated with group size in primate species and considered strong evidence for the social brain hypothesis. Our results suggest that spontaneous eye-blinks have acquired a role in social communication, similar to grooming, to adapt to complex social living during primate evolution.
Both human and nonhuman primates have been suggested to possess some essential knowledge about animate entities, but it remains unclear whether the concept of animacy is shared across species, which properties are used as an "animacy marker," and whether such ability is present at birth. We investigated infant Japanese monkeys looking responses towards novel objects varying in both physical appearance and self-propelled motion, with the aim of depicting the role of eyes and fluffiness in the early recognition of animacy. Presented with an inanimate natural stone, three-month-old monkeys showed longer looking times at the stones self-propelled motion than at its baseline still posture. This effect became significantly smaller when artificial fur was attached to the stone, while adding artificial eyes did not elicit a departing pattern in their looking behavior. In contrast, one-month-old monkeys showed no systematic differences in their looking behavior. This suggests that the concept of animacy in terms of self-propelledness may develop between one and three months of age, with sensitivity to texture emerging by three months. Development of biological knowledge is discussed in relation to social knowledge from both ontogenetic and phylogenetic perspectives.
Although an extensive body of literature exists on the cognitive underpinnings of gaze movements in macaques and humans, few studies have investigated this topic from a broader evolutionary perspective. This study used the gap-overlap paradigm to examine the timing of the gaze movements by four hominid species: humans, chimpanzees, gorillas, and orangutans. The saccade latency involved in shifting the gaze from central to peripheral stimuli was measured and compared under two conditions, gap and overlap. The central stimulus disappeared shortly before the onset of the peripheral stimulus under the gap condition, but it remained under the overlap condition. Although all species demonstrated similar saccade latencies under the gap condition, the species clearly differed from one another under the overlap condition, which may suggest their similar perceptual and motor mechanism of making a saccade on the one hand and their differential strategies for coping with the competition between two activities involving fixation and initiation of a saccade (i.e. central vs. peripheral visual stimuli) on the other hand. In particular, humans showed longer saccade latency under the overlap condition compared to the other great apes, which may reflect this species unique means of visual processing.
How do humans and their closest relatives, chimpanzees, differ in their fundamental abilities for seeing the visual world? In this study, we directly compared the gaze movements of humans and the closest species, chimpanzees, using an eye-tracking system. During free viewing of a naturalistic scene, chimpanzees made more fixations per second (up to four) than did humans (up to three). This species difference was independent of the semantic variability of the presented scenes. The gap-overlap paradigm revealed that, rather than resulting from the sensitivity to the peripherally presented stimuli per se, the species difference reflected the particular strategy each species employed to solve the rivalry between central (fixated) and peripheral stimuli in their visual fields. Finally, when presented with a movie in which small images successively appeared/disappeared at random positions at the chosen presentation rate, chimpanzees tracked those images at the point of fixation for a longer time than did humans, outperforming humans in their speed of scanning. Our results suggest that chimpanzees and humans differ quantitatively in their visual strategies involving the timing of gaze movement. We discuss the functional reasons for each species employing such specific strategies.
The ability to distinguish actions and effects caused by oneself from events occurring in the external environment is a fundamental aspect of human cognition. Underlying such distinctions, self-monitoring processes are often assumed, in which predicted events accompanied by ones own volitional action are compared with actual events observed in the external environment. Although many studies have examined the absence or presence of a certain type of self-recognition (i.e. mirror self-recognition) in non-human animals, the underlying cognitive mechanisms remain unclear. Here, we provide, to our knowledge, the first behavioural evidence that chimpanzees can perform self/other distinction for external events on the basis of self-monitoring processes. Three chimpanzees were presented with two cursors on a computer display. One cursor was manipulated by a chimpanzee using a trackball, while the other displayed motion that had been produced previously by the same chimpanzee. Chimpanzees successfully identified which cursor they were able to control. A follow-up experiment revealed that their performance could not be explained by simple associative responses. A further experiment with one chimpanzee showed that the monitoring process occurred in both temporal and spatial dimensions. These findings indicate that chimpanzees and humans share the fundamental cognitive processes underlying the sense of being an independent agent.
The stream/bounce display represents an ambiguous motion event in which two identical visual objects move toward one another and the objects overlap completely before they pass each another. In our perception, they can be interpreted as either streaming past one another or bouncing off each other. Previous studies have shown that the streaming percept of the display is generic for humans, suggesting the inertial nature of the motion integration process. In this study, chimpanzees took part in behavioral experiments using an object-tracking task to reveal the characteristics of their stream/bounce perception. Chimpanzees did not show a tendency toward a dominant "stream" perception of the stream/bounce stimulus. However, depth cues, such as X-junctions and local motion coherence, did promote the stream percept in chimpanzees. These results suggest both similarities and differences between chimpanzees and humans with respect to motion integration and object individuation processes.
Five-year-old Japanese monkeys were tested on long-term visual recognition memory. The objects used were those that they had encountered daily during their first 2 years of life as to-be-remembered stimuli: persons, peers, and places. After a 3-year delay, we conducted a recognition test using the preferential looking paradigm where the monkeys were presented with pictures of these familiar stimuli in combination with those of novel stimuli. The monkeys looked relatively longer at pictures of familiar stimuli than at those of novel stimuli, while participants in the control group, who had never seen the stimuli in question, showed no discriminative preference. The monkeys thus recognized the familiar stimuli through the pictures, suggesting retention of visual information on real objects encountered in their lives even after a 3-year delay. Our present findings confirmed long-term visual recognition in monkeys, which might be essential to ecologically and socially significant behaviors such as individual identification.
Previous studies comparing eye movements between humans and their closest relatives, chimpanzees, have revealed similarities and differences between the species in terms of where individuals fixate their gaze during free viewing of a naturalistic scene, including social stimuli (e.g. body and face). However, those results were somewhat confounded by the fact that gaze behavior is influenced by low-level stimulus properties (e.g., color and form) and by high-level processes such as social sensitivity and knowledge about the scene. Given the known perceptual and cognitive similarities between chimpanzees and humans, it is expected that such low-level effects do not play a critical role in explaining the high-level similarities and differences between the species. However, there is no quantitative evidence to support this assumption. To estimate the effect of local stimulus saliency on such eye-movement patterns, this study used a well-established bottom-up saliency model. In addition, to elucidate the cues that the viewers use to guide their gaze, we presented scenes in which we had manipulated various stimulus properties. As expected, the saliency model did not fully predict the fixation patterns actually observed in chimpanzees and humans. In addition, both species used multiple cues to fixate socially significant areas such as the face. There was no evidence suggesting any differences between chimpanzees and humans in their responses to low-level saliency. Therefore, this study found a substantial amount of similarity in the perceptual mechanisms underlying gaze guidance in chimpanzees and humans and thereby offers a foundation for direct comparisons between them.
A comparison of developmental patterns of white matter (WM) within the prefrontal region between humans and nonhuman primates is key to understanding human brain evolution. WM mediates complex cognitive processes and has reciprocal connections with posterior processing regions [1, 2]. Although the developmental pattern of prefrontal WM in macaques differs markedly from that in humans , this has not been explored in our closest evolutionary relative, the chimpanzee. The present longitudinal study of magnetic resonance imaging scans demonstrated that the prefrontal WM volume in chimpanzees was immature and had not reached the adult value during prepuberty, as observed in humans but not in macaques. However, the rate of prefrontal WM volume increase during infancy was slower in chimpanzees than in humans. These results suggest that a less mature and more protracted elaboration of neuronal connections in the prefrontal portion of the developing brain existed in the last common ancestor of chimpanzees and humans, and that this served to enhance the impact of postnatal experiences on neuronal connectivity. Furthermore, the rapid development of the human prefrontal WM during infancy may help the development of complex social interactions, as well as the acquisition of experience-dependent knowledge and skills to shape neuronal connectivity.
The sound of ones own name is one of the most salient auditory environmental stimuli. Several studies of human brain potentials have revealed some characteristic waveforms when we hear our own names. In a recent work, we investigated event-related potentials (ERPs) in a female chimpanzee and demonstrated that the ERP pattern generated when she heard her own name differed from that generated when she heard other sounds. However, her ERPs did not exhibit a prominent positive shift around 300 ms (P3) in response to her own name, as has been repeatedly shown in studies of human ERPs. The present study collected comparative data for adult humans using basically the same procedure as that used in our previous study of the chimpanzee. These results also revealed no prominent P3 to the human subjects own names. The lack of increased P3 is therefore likely due to our experimental protocol, in which we presented the subjects own name relatively frequently. In contrast, our results revealed prominent negativity to the subjects own name at around 500 ms in the chimpanzee and around 200 ms in human subjects. This may indicate that initial orientation to the sound of ones own name is delayed in the chimpanzee.
Twenty-two pairs of typically developing toddlers (M=24.32 months) and their mothers were observed in a play-room solving puzzles during 30 min. The target of the observations was hand-taking gesture. Researchers have thought that this gesture is rare among typically developing children and is more frequent among autistic children. Ten in 22 children showed this gesture in only 30 min. They should know "I can not do it by myself, but my mother can do it." When we can assume that children know others mental mechanism, it might be the origins of a theory of mind.
In mammals, bitter taste is mediated by T2R genes, which belong to the large family of seven transmembrane G protein-coupled receptors. Because T2Rs are directly involved in the interaction between mammals and their dietary sources, it is likely that these genes evolved to reflect species specific diets during mammalian evolution. Here, we investigated the sequences of all 28 putative functional chimpanzee T2R genes (cT2Rs) in 46 western chimpanzees to compare the intraspecies variations in chimpanzees to those already known for all 25 human functional T2R genes (hT2Rs). The numbers of functional genes varied among individuals in western chimpanzees, and most chimpanzees had two or three more functional genes than humans. Similarly to hT2Rs, cT2Rs showed high nucleotide diversity along with a large number of amino acid substitutions. Comparison of the nucleotide substitution patterns in cT2Rs with those in five cT2R pseudogenes and 14 autosomal intergenic noncoding regions among the same individuals revealed that the evolution of cT2R genes was almost identical to that of putative neutral regions with slight but significantly positive Tajimas D values, suggesting that selective constraint on these genes was relaxed with weak balancing selection. These trends have resulted in the occurrence of various divergent alleles of T2Rs within the western chimpanzee populations and in heterozygous individuals who might have the ability to taste a broader range of substances.
Real-life situations provide rich sets of cues that viewers evaluate in terms of their emotional significance. In this study, chimpanzees (Pan troglodytes) viewed a movie depicting naturalistic scenes involving the whole-body expressions of conspecifics to examine how nonhuman primates perceived the combination of these cues and how each cue contributed to the overall perception. Viewing time was measured while the chimpanzees watched movie clips without sound. Among scenes depicting neutrality, general excitement, agonism, and playfulness, chimpanzees looked longest at those depicting agonism. This bias toward agonistic scenes may indicate an attentional sensitivity toward threat/fear-related negative situations among chimpanzees. The effect disappeared when the images were scrambled, ruling out the possible effect of pixel-level properties on the results. In addition, the follow-up analyses revealed that the effect was independent of the presentation order and of the number of individuals in each clip. The manipulation of playback speeds had little effect on the looking times. The elimination of facial cues slightly influenced the looking times but did not change the strong bias toward agonistic scenes. This robustness of the main effect against image manipulations may indicate that the chimpanzees attended directly to the contextual information implied by the cues rather than to the cues per se (e.g., facial expressions, speed of movements).
The neural system of our closest living relative, the chimpanzee, is a topic of increasing research interest. However, electrophysiological examinations of neural activity during visual processing in awake chimpanzees are currently lacking.
Previous studies have shown that a variety of animals including humans are sensitive to social cues from others and shift their attention to the same objects attended to by others. However, little is known about how animals process conspecifics and another species actions, although primates recognize conspecific faces better than those of another species. In this study, using unrestrained eye-tracking techniques, we first demonstrated that conspecific social cues modulated looking behaviours of chimpanzees more than human cues, whereas human observers were equally sensitive to both species. Additionally, first pass gaze duration at the face indicates that chimpanzees looked at the chimpanzees face longer than the human face, suggesting that chimpanzees might extract more referential information from a conspecific face. These results also imply that a unique ability for extracting referential information from a variety of social objects has emerged during human evolution.
Humans readily perceive whole shapes as intact when some portions of these shapes are occluded by another object. This type of amodal completion has also been widely reported among nonhuman animals and is related to pictorial depth perception. However, the effect of a cast shadow, a critical pictorial-depth cue for amodal completion has been investigated only rarely from the comparative-cognitive perspective. In the present study, we examined this effect in chimpanzees and humans.
Humans detect faces with direct gazes among those with averted gazes more efficiently than they detect faces with averted gazes among those with direct gazes. We examined whether this "stare-in-the-crowd" effect occurs in chimpanzees (Pan troglodytes), whose eye morphology differs from that of humans (i.e., low-contrast eyes, dark sclera).
We conducted three experiments to investigate how object-based components contribute to the attentional processes of chimpanzees and to examine how such processes operate with regard to perceptually structured objects. In Experiment 1, chimpanzees responded to a spatial cueing task that required them to touch a target appearing at either end of two parallel rectangles. We compared the time involved in shifting attention (cost of attentional shift) when the locations of targets were cued and non cued. Results showed that the cost of the attentional shift within one rectangle was smaller than that beyond the objects boundary, demonstrating object-based attention in chimpanzees. The results of Experiment 2, conducted with different stimulus configurations, replicated the results of Experiment 1, supporting that object-based attention operates in chimpanzees. In Experiment 3, the cost of attentional shift within a cued but partly occluded rectangle was shorter than that within a rectangle that was cued but divided in the middle. The results suggest that the attention of chimpanzees is activated not only by an explicit object but also by fragmented patches represented as an object at a higher-order perceptual level. Chimpanzees object-based attention may be similar to that of humans.
The brain activity of a fully awake chimpanzee being presented with her name was investigated. Event-related potentials (ERPs) were measured for each of the following auditory stimuli: the vocal sound of the subjects own name (SON), the vocal sound of a familiar name of another group member, the vocal sound of an unfamiliar name and a non-vocal sound. Some differences in ERP waveforms were detected between kinds of stimuli at latencies at which P3 and Nc components are typically observed in humans. Following stimulus onset, an Nc-like negative shift at approximately 500 ms latency was observed, particularly in response to SON. Such specific ERP patterns suggest that the chimpanzee processes her name differently from other sounds.
Previous studies have reported that backgrounds depicting linear perspective and texture gradients influence relative size discrimination in nonhuman animals (known as the "corridor illusion"), but research has not yet identified the other kinds of depth cues contributing to the corridor illusion. This study examined the effects of linear perspective and shadows on the responses of a chimpanzee (Pan troglodytes) to the corridor illusion. The performance of the chimpanzee was worse when a smaller object was presented at the farther position on a background reflecting a linear perspective, implying that the corridor illusion was replicated in the chimpanzee (Imura, Tomonaga, & Yagi, 2008). The extent of the illusion changed as a function of the position of the shadows cast by the objects only when the shadows were moving in synchrony with the objects. These findings suggest that moving shadows and linear perspective contributed to the corridor illusion in a chimpanzee.
To examine how gestural cues trigger shifts in attention, two chimpanzees and ten humans participated in a computer-controlled target-detection experiment. Before presenting the target at either a left or right location, a photograph of a human gesturing towards or away from the forthcoming target location was presented on a CRT display monitor. Humans exhibited faster response times in the trials in which the gestural cue signalled the target location (valid trials) as opposed to the opposite location (invalid trials) when the cue-target interval (stimulus onset asynchrony, SOA) was 100 ms but not when the SOA was 500 ms. However, chimpanzees showed faster response times in valid trials than in invalid trials only when the SOA was 500 ms. The reflexive mechanism is known to activate attention quickly, while the slow onset of the cueing effect can be considered a sign of voluntary control of attentional shift. The present study used the cueing paradigm and a comparative cognitive perspective to clarify the effect of directional gestural cues for the first time. The results suggested that different mechanisms underlie the attentional shift triggered by gestural cues in humans and chimpanzees.
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.
Detection of others gaze direction is an essential tool in everyday communication. As the gaze direction is analyzed rapidly and automatically, we hardly notice how we are performing this task. Wollastons illusion [Wollaston, W. H. (1824). On the apparent direction of eye in a portrait. Philosophical Transactions of the Royal Society of London Series B, 114, 247-256] provides us the chance to understand an aspect of this problem, in which the change in orientation of the face results in the shift of the perceived gaze direction. This illusion suggests that we analyze others gaze directions by integrating information from eyes and that from face. By using Wollastons illusion, we examined how 6- to 8-month-old infants process gaze direction in upright and inverted faces. Our results suggest that 8-month-olds process gaze direction in terms of the orientation of the face, and perceive an illusory shift of the gaze direction in Wollastons illusion when the face was shown in an upright orientation.
In a previous study, Adachi, Kuwahata, Fujita, Tomonaga & Matsuzawa demonstrated that infant Japanese macaques (Macaca fuscata) form cross-modal representations of conspecifics but not of humans. However, because the subjects in the experiment were raised in a large social group and had considerably less exposure to humans than to conspecifics, it was an open question whether their lack of cross-modal representation of humans simply reflected their lower levels of exposure to humans or was caused by some innate restrictions on the ability. To answer the question, we used the same procedure but tested infant Japanese macaques with more extensive experience of humans in daily life. Briefly, we presented monkeys with a photograph of either a monkey or a human face on an LCD monitor after playing a vocalization of one of these two species. The subjects looked at the monitor longer when a voice and a face were mismatched than when they were matched, irrespective of whether the preceding vocalization was a monkeys or a humans. This suggests that once monkeys have extensive experience with humans, they will form a cross-modal representation of humans as well as of conspecifics.
Five infants were observed longitudinally. In over 30 h of observations, seven spontaneous smiles and one spontaneous laugh were found. All smiles were observed in infants between the ages of 10 and 15 months. These data indicate that spontaneous smiles do not disappear at 2 months of age and they still exist at over 15 months. This disproves some emotional expression theories, where spontaneous smiles are considered to be precursor to and replaced by social smiles. Our data suggest that those theories must be revised and provide new perspectives on this field of studies.
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.
Faces, as socially relevant stimuli, readily capture human visuospatial attention. Although faces also play important roles in the social lives of chimpanzees, the closest living species to humans, the way in which faces are attentionally processed remains unclear from a comparative-cognitive perspective. In the present study, three young chimpanzees (Pan troglodytes) were tested with a simple manual response task in which various kinds of photographs, including faces as non-informative cues, were followed by a target.
Developmental prolongation is thought to contribute to the remarkable brain enlargement observed in modern humans (Homo sapiens). However, the developmental trajectories of cerebral tissues have not been explored in chimpanzees (Pan troglodytes), even though they are our closest living relatives. To address this lack of information, the development of cerebral tissues was tracked in growing chimpanzees during infancy and the juvenile stage, using three-dimensional magnetic resonance imaging and compared with that of humans and rhesus macaques (Macaca mulatta). Overall, cerebral development in chimpanzees demonstrated less maturity and a more protracted course during prepuberty, as observed in humans but not in macaques. However, the rapid increase in cerebral total volume and proportional dynamic change in the cerebral tissue in humans during early infancy, when white matter volume increases dramatically, did not occur in chimpanzees. A dynamic reorganization of cerebral tissues of the brain during early infancy, driven mainly by enhancement of neuronal connectivity, is likely to have emerged in the human lineage after the split between humans and chimpanzees and to have promoted the increase in brain volume in humans. Our findings may lead to powerful insights into the ontogenetic mechanism underlying human brain enlargement.
Because the faces and eyes of primates convey a rich array of social information, the way in which primates view faces and eyes reflects species-specific strategies for facial communication. How are humans and closely related species such as great apes similar and different in their viewing patterns for faces and eyes? Following previous studies comparing chimpanzees (Pan troglodytes) with humans (Homo sapiens), this study used the eye-tracking method to directly compare the patterns of face and eye scanning by humans, gorillas (Gorilla gorilla), and orangutans (Pongo abelii). Human and ape participants freely viewed pictures of whole bodies and full faces of conspecifics and allospecifics under the same experimental conditions. All species were strikingly similar in that they viewed predominantly faces and eyes. No particular difference was identified between gorillas and orangutans, and they also did not differ from the chimpanzees tested in previous studies. However, humans were somewhat different from apes, especially with respect to prolonged eye viewing. We also examined how species-specific facial morphologies, such as the male flange of orangutans and the black-white contrast of human eyes, affected viewing patterns. Whereas the male flange of orangutans affected viewing patterns, the color contrast of human eyes did not. Humans showed prolonged eye viewing independently of the eye color of presented faces, indicating that this pattern is internally driven rather than stimulus dependent. Overall, the results show general similarities among the species and also identify unique eye-viewing patterns in humans.
It is important to monitor feedback related to the intended result of an action while executing that action. This monitoring process occurs hierarchically; that is, sensorimotor processing occurs at a lower level, and conceptual representation of action goals occurs at a higher level. Although the hierarchical nature of self-monitoring may derive from the evolutionary history of humans, little is known about this cognitive process in non-human primates. This study showed that the relative contributions of kinematic information and goal representations to self-monitoring differ for chimpanzees and humans. Both species performed aiming actions whereby participants moved a cursor to hit targets. Additionally, a distractor cursor was presented simultaneously, and participants discriminated the cursor under their control from the cursor not under their control. The results showed that chimpanzees found it difficult to determine whether they were controlling the distractor when it moved toward the target, even though the distractors kinematics and the participants actions were dissociated. In contrast, humans performed efficiently regardless of any overlap between the presumptive and observed goals of the action. Our results suggest that goal representation, rather than motor kinematics, is the primary source of information for self-monitoring in chimpanzees, whereas humans efficiently integrate both dimensions of information. Our results are consistent with evidence showing species differences during imitation of others actions, and suggest that humans have evolved the cognitive capacity to monitor motor kinematics in a more flexible manner than have chimpanzees.
Emerging infectious diseases (EIDs) in wildlife are major threats both to human health and to biodiversity conservation. An estimated 71.8 % of zoonotic EID events are caused by pathogens in wildlife and the incidence of such diseases is increasing significantly in humans. In addition, human diseases are starting to infect wildlife, especially non-human primates. The chimpanzee is an endangered species that is threatened by human activity such as deforestation, poaching, and human disease transmission. Recently, several respiratory disease outbreaks that are suspected of having been transmitted by humans have been reported in wild chimpanzees. Therefore, we need to study zoonotic pathogens that can threaten captive chimpanzees in primate research institutes. Serological surveillance is one of several methods used to reveal infection history. We examined serum from 14 captive chimpanzees in Japanese primate research institutes for antibodies against 62 human pathogens and 1 chimpanzee-borne infectious disease. Antibodies tested positive against 29 pathogens at high or low prevalence in the chimpanzees. These results suggest that the proportions of human-borne infections may reflect the chimpanzees history, management system in the institute, or regional epidemics. Furthermore, captive chimpanzees are highly susceptible to human pathogens, and their induced antibodies reveal not only their history of infection, but also the possibility of protection against human pathogens.
Six strains, TKU 25, TKU 28, TKU 30, TKU 31(T), TKU 33 and TKU 34, were isolated from the oral cavity of a chimpanzee (Pan troglodytes). Colonies of strains grown on Mitis-Salivarius agar were similar in morphology to that of Streptococcus mutans. The novel strains were Gram-stain-positive, facultatively anaerobic cocci that lacked catalase activity. Analysis of the partial 16S rRNA gene sequences of these isolates showed that the most closely related strain was the type strain of S. mutans (96.4?%). The next closely related strains to the isolates were the type strains of Streptococcus devriesei (94.5?%) and Streptococcus downei (93.9?%). These isolates could be distinguished from S. mutans by inulin fermentation and alkaline phosphatase activity (API ZYM system). The peptidoglycan type of the novel isolates was Glu-Lys-Ala(3). Strains were not susceptible to bacitracin. On the basis of phenotypic characterization, partial 16S rRNA gene and two housekeeping gene (groEL and sodA) sequence data, we propose a novel taxon, Streptococcus troglodytae sp. nov.; the type strain is TKU 31(T) (?=?JCM 18038(T)?=?DSM 25324(T)).
We examined the perceptions of emergent configurations in humans and chimpanzees using a target-localization task. The stimulus display consisted of a target placed among multiple identical distractors. The target and distractors were presented either solely, within congruent contexts in which salient configurations emerge, or within incongruent contexts in which salient configurations do not emerge. We found that congruent contexts had similar facilitative effects on target localization by humans and chimpanzees, whereas similar disruptive effects emerged when the stimuli were presented within incongruent contexts. When display size was manipulated, targets under the congruent-context condition were localized in a parallel manner, but those under the no-context and incongruent-context conditions were localized in a serial manner by both species. These results suggest that both humans and chimpanzees perceive emergent configurations when targets and distractors are presented within certain congruent contexts and that they process such emergent configurations preattentively.
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