Cross-species variation in gaze following and conspecific preference among great apes, human infants and adults

Although previous studies have shown that many species follow gaze, few have directly compared closely related species, and thus its cross-species variation remains largely unclear. In this study, we compared three great ape species (bonobos, Pan paniscus, chimpanzees, Pan troglodytes, orang-utans, Pongo abelii) and humans (12-month-olds and adults) in their gaze-following responses to the videos of conspecific and allospecific models. In the video, the model turned his head repeatedly to one of two identical objects. We used a noninvasive eye-tracking technique to measure participants' eye movements, and used both conspecific and allospecific models as stimuli to examine their potential preference in following conspecific rather than allospecific gaze. Experiment 1 presented to great apes the videos of conspecific and human models. We found that all species followed the conspecific gaze. Chimpanzees did not follow the human gaze, whereas bonobos did. Bonobos reacted overall more sensitively than chimpanzees to both conspecific and human gaze. Experiment 2 presented to human infants and adults the videos of human, chimpanzee and orang-utan models. Both infants and adults followed the human gaze. Unlike adults, infants did not follow the ape gaze. Experiment 3 presented to great apes the videos of allospecific ape models. Consistent with experiment 1, chimpanzees did not follow the allospecific ape gaze, whereas bonobos and orang-utans did. Importantly, preferential following of conspecific gaze by chimpanzees (experiment 1) and human infants (experiment 2) was mainly explained by their prolonged viewing of the conspecific face and thus seems to reflect their motivation to attend selectively to the conspecific models. Taken together, we conclude that gaze following is modulated by both subject species and model species in great apes and humans, presumably a reflection of the subjects' intrinsic sensitivity to gaze and also their selective interest in particular models. (C) 2014 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.PostprintPeer reviewe

Spontaneous attention and psycho-physiological responses to others’ injury in chimpanzees

他者の怪我に対しチンパンジーが情動的に反応することを発見 --最新技術が明かす類人猿の注意と生理的反応--. 京都大学プレスリリース. 2019-06-19.Previous studies have shown that humans experience negative emotions when seeing contextual cues of others’ pain, such as injury (i.e., empathic pain), even without observing behavioral expressions of distress. However, this phenomenon has not been examined in nonhuman primates. We tested six chimpanzees (Pan troglodytes) to experimentally examine their reactions to others’ injury. First, we measured viewing responses using eye-tracking. Chimpanzees spontaneously attended to injured conspecifics more than non-injured conspecifics, but did not do so in a control condition in which images of injuries were scrambled while maintaining color information. Chimpanzees did not avoid viewing injuries at any point during stimulus presentation. Second, we used thermal imaging to investigate chimpanzees’ physiological responses to others’ injury. Previous studies reported that reduced nasal temperature is a characteristic of arousal, particularly arousal associated with negative valence. We presented chimpanzees with a realistic injury: a familiar human experimenter with a prosthetic wound and artificial running blood. Chimpanzees exhibited a greater nasal temperature reduction in response to injury compared with the control stimulus. Finally, chimpanzees were presented with a familiar experimenter who stabbed their (fake) thumb with a needle, with no running blood, a situation that may be more challenging in terms of understanding the cause of distress. Chimpanzees did not physiologically distinguish this condition from the control condition. These results suggest that chimpanzees inspect others’ injuries and become aroused by seeing injuries even without observing behavioral cues, but have difficulty doing so without explicit (or familiar) cues (i.e., open wound and blood)

Eye tracking uncovered great apes' ability to anticipate that other individuals will act according to false beliefs

Financial support came from Ministry of Education, Culture, Sports, Science and Technology (K-CONNEX to FK), Japan Society for Promotion of Science (KAKENHI 26885040, 16K21108 to FK), National Science Foundation (DGE-1106401 to CK), JSPS (KAKENHI 26245069, 24000001 to SH), and European Research Council (Synergy grant 609819 SOMICS to JC)Using a novel eye-tracking test, we recently showed that great apes anticipate that other individuals will act according to false beliefs. This finding suggests that, like humans, great apes understand others' false beliefs, at least in an implicit way. One key question raised by our study is why apes have passed our tests but not previous ones. In this article, we consider this question by detailing the development of our task. We considered three major differences in our task compared to the previous ones. First, we monitored apes' eye movements, and specifically their anticipatory looks, in order to measure their predictions about how agents will behave. Second, we adapted our design from an anticipatory-looking false belief test originally developed for human infants. Third, we developed novel test scenarios that were specifically designed to capture the attention of our ape participants. We then discuss how each difference may help explain differences in performance on our task and previous ones, and finally propose some directions for future studies.Publisher PDFPeer reviewe

Nasal temperature drop in response to a playback of conspecific fights in chimpanzees : a thermo-imaging study

This study was conducted in part under the first author's postdoc program; the Japan Society for Promotion of Science (JSPS) for study abroad. FK and SH respectively received JSPS KAKENHI Grant Number 26885040 and 26245069. This study was also in part funded by JSPS MEXT KAKENHI Grant Number 24000001, JSPS-LGP-U04, JSPS core-to-core type A CCSN, and MEXT-PRI-Human Evolution.Emotion is one of the central topics in animal studies and is likely to attract attention substantially in the coming years. Recent studies have developed a thermo-imaging technique to measure the facial skin temperature in the studies of emotion in humans and macaques. Here we established the procedures and techniques needed to apply the same technique to great apes. We conducted two experiments respectively in the two established research facilities in Germany and Japan. Total twelve chimpanzees were tested in three conditions in which they were presented respectively with the playback sounds (Exp. 1) or the videos (Exp. 2) of fighting conspecifics, control sounds/videos (allospecific display call: Exp. 1; resting conspecifics: Exp. 2), and no sound/image. Behavioral, hormonal (salivary cortisol) and heart-rate responses were simultaneously recorded. The nasal temperature of chimpanzees linearly dropped up to 1.5. °C in 2. min, and recovered to the baseline in 2. min, in the experimental but not control conditions. We found the related changes in excitement behavior and heart-rate variability, but not in salivary cortisol, indicating that overall responses were involved with the activities of sympathetic nervous system but not with the measureable activities of the hypothalamus-pituitary-adrenal (HPA) axis. The influence of general activity (walking, eating) was not negligible but controllable in experiments. We propose several techniques to control those confounding factors. Overall, thermo-imaging is a promising technique that should be added to the traditional physiological and behavioral measures in primatology and comparative psychology.PostprintPeer reviewe

Great apes anticipate that other individuals will act according to false beliefs

Financial support came from NSFGRFP DGE-1106401 (CK), MEXT K-CONNEX, JSPS KAKENHI 26885040, 16K21108 (FK), JSPS KAKENHI 26245069, 24000001 (SH), and ERC-Synergy grant 609819 (JC).Humans operate with a "theory-of-mind" with which they understand that others’ actions are driven not by reality but by beliefs about reality, even when those beliefs are false. Although great apes share with humans many social-cognitive skills, they have repeatedly failed experimental tests of such false belief understanding. Using an anticipatory looking test (originally developed for human infants), we show that three species of great apes reliably look in anticipation of an agent acting on a location where he falsely believes an object to be, even though they themselves know that it is no longer there. These results suggest that great apes also operate—at least on an implicit level—with an understanding of false beliefs.PostprintPostprintPeer reviewe

A test of the submentalizing hypothesis : apes' performance in a false belief task inanimate control

Financial support came from Ministry of Education, Culture, Sports, Science and Technology (K-CONNEX to FK), Japan Society for Promotion of Science (KAKENHI 26885040, 16K21108 to FK), JSPS (KAKENHI 26245069, 24000001 to SH), and European Research Council (Synergy grant 609819 SOMICS to JC).Much debate concerns whether any nonhuman animals share with humans the ability to infer others' mental states, such as desires and beliefs. In a recent eye-tracking false-belief task, we showed that great apes correctly anticipated that a human actor would search for a goal object where he had last seen it, even though the apes themselves knew that it was no longer there. In response, Heyes proposed that apes' looking behavior was guided not by social cognitive mechanisms but rather domain-general cueing effects, and suggested the use of inanimate controls to test this alternative submentalizing hypothesis. In the present study, we implemented the suggested inanimate control of our previous false-belief task. Apes attended well to key events but showed markedly fewer anticipatory looks and no significant tendency to look to the correct location. We thus found no evidence that submentalizing was responsible for apes' anticipatory looks in our false-belief task.Publisher PDFPeer reviewe

Otto A. Weber (1924.-1994.)

Many unique features of human communication, cooperation, and culture depend on theory of mind, the ability to attribute mental states to oneself and others. But is theory of mind uniquely human? Nonhuman animals, such as humans’} closest ape relatives, have succeeded in some theory-of-mind tasks; however, it remains disputed whether they do so by reading others{’} minds or their behavior. Here, we challenged this behavior-rule account using a version of the goggles test, incorporated into an established anticipatory-looking false-belief task with apes. We provide evidence that, in the absence of behavioral cues, apes consulted their own past experience of seeing or not seeing through a novel barrier to determine whether an agent could see through the same barrier.Human social life depends on theory of mind, the ability to attribute mental states to oneself and others. A signature of theory of mind, false belief understanding, requires representing others{’} views of the world, even when they conflict with one{’}s own. After decades of research, it remains controversial whether any nonhuman species possess a theory of mind. One challenge to positive evidence of animal theory of mind, the behavior-rule account, holds that animals solve such tasks by responding to others{’} behavioral cues rather than their mental states. We distinguish these hypotheses by implementing a version of the {“}goggles{”} test, which asks whether, in the absence of any additional behavioral cues, animals can use their own self-experience of a novel barrier being translucent or opaque to determine whether another agent can see through the same barrier. We incorporated this paradigm into an established anticipatory-looking false-belief test for great apes. In a between-subjects design, apes experienced a novel barrier as either translucent or opaque, although both looked identical from afar. While being eye tracked, all apes then watched a video in which an actor saw an object hidden under 1 of 2 identical boxes. The actor then scuttled behind the novel barrier, at which point the object was relocated and then removed. Only apes who experienced the barrier as opaque visually anticipated that the actor would mistakenly search for the object in its previous location. Great apes, therefore, appeared to attribute differential visual access based specifically on their own past perceptual experience to anticipate an agent{’s actions in a false-belief test

Bonobos and chimpanzees remember familiar conspecifics for decades

Funding: We are grateful to the Royal Zoological Society of Scotland (RZSS) for core financial support to the RZSS Edinburgh Zoo’s Budongo Research Unit where this project was carried out.Recognition and memory of familiar conspecifics provides the foundation for complex sociality and is vital to navigating an unpredictable social world [Tibbetts and Dale, Trends Ecol. Evol. 22 , 529–537 (2007)]. Human social memory incorporates content about interactions and relationships and can last for decades [Sherry and Schacter, Psychol. Rev. 94 , 439–454 (1987)]. Long-term social memory likely played a key role throughout human evolution, as our ancestors increasingly built relationships that operated across distant space and time [Malone et al., Int. J. Primatol. 33 , 1251–1277 (2012)]. Although individual recognition is widespread among animals and sometimes lasts for years, little is known about social memory in nonhuman apes and the shared evolutionary foundations of human social memory. In a preferential-looking eye-tracking task, we presented chimpanzees and bonobos (N = 26) with side-by-side images of a previous groupmate and a conspecific stranger of the same sex. Apes’ attention was biased toward former groupmates, indicating long-term memory for past social partners. The strength of biases toward former groupmates was not impacted by the duration apart, and our results suggest that recognition may persist for at least 26 y beyond separation. We also found significant but weak evidence that, like humans, apes may remember the quality or content of these past relationships: apes’ looking biases were stronger for individuals with whom they had more positive histories of social interaction. Long-lasting social memory likely provided key foundations for the evolution of human culture and sociality as they extended across time, space, and group boundaries.Publisher PDFPeer reviewe

3D-MuPPET: 3D Multi-Pigeon Pose Estimation and Tracking

Markerless methods for animal posture tracking have been developing recently, but frameworks and benchmarks for tracking large animal groups in 3D are still lacking. To overcome this gap in the literature, we present 3D-MuPPET, a framework to estimate and track 3D poses of up to 10 pigeons at interactive speed using multiple-views. We train a pose estimator to infer 2D keypoints and bounding boxes of multiple pigeons, then triangulate the keypoints to 3D. For correspondence matching, we first dynamically match 2D detections to global identities in the first frame, then use a 2D tracker to maintain correspondences accross views in subsequent frames. We achieve comparable accuracy to a state of the art 3D pose estimator for Root Mean Square Error (RMSE) and Percentage of Correct Keypoints (PCK). We also showcase a novel use case where our model trained with data of single pigeons provides comparable results on data containing multiple pigeons. This can simplify the domain shift to new species because annotating single animal data is less labour intensive than multi-animal data. Additionally, we benchmark the inference speed of 3D-MuPPET, with up to 10 fps in 2D and 1.5 fps in 3D, and perform quantitative tracking evaluation, which yields encouraging results. Finally, we show that 3D-MuPPET also works in natural environments without model fine-tuning on additional annotations. To the best of our knowledge we are the first to present a framework for 2D/3D posture and trajectory tracking that works in both indoor and outdoor environments

Human ostensive signals do not enhance gaze following in chimpanzees, but do enhance object-oriented attention

Financial support came from Ministry of Education, Culture, Sports, Science and Technology [K-CONNEX to FK], Japan Society for Promotion of Science KAKENHI 26885040, 16K21108, and 18H05072 to FK, 26245069, 16H06301, 16H06283, and 18H05524 to SH, 15H05709, 16H06238, and JSPS-CCSN to MT, and JSPS-LGP-U04 and Great Ape Information Network to SH and MT, and the European Research Council [SOMICS 609819 to JC].The previous studies have shown that human infants and domestic dogs follow the gaze of a human agent only when the agent has addressed them ostensively—e.g., by making eye contact, or calling their name. This evidence is interpreted as showing that they expect ostensive signals to precede referential information. The present study tested chimpanzees, one of the closest relatives to humans, in a series of eye-tracking experiments using an experimental design adapted from these previous studies. In the ostension conditions, a human actor made eye contact, called the participant’s name, and then looked at one of two objects. In the control conditions, a salient cue, which differed in each experiment (a colorful object, the actor’s nodding, or an eating action), attracted participants’ attention to the actor’s face, and then the actor looked at the object. Overall, chimpanzees followed the actor’s gaze to the cued object in both ostension and control conditions, and the ostensive signals did not enhance gaze following more than the control attention-getters. However, the ostensive signals enhanced subsequent attention to both target and distractor objects (but not to the actor’s face) more strongly than the control attention-getters—especially in the chimpanzees who had a close relationship with human caregivers. We interpret this as showing that chimpanzees have a simple form of communicative expectations on the basis of ostensive signals, but unlike human infants and dogs, they do not subsequently use the experimenter’s gaze to infer the intended referent. These results may reflect a limitation of non-domesticated species for interpreting humans’ ostensive signals in inter-species communication.PostprintPeer reviewe