An investigation on the olfactory capabilities of domestic dogs (Canis lupus familiaris).

The extraordinary olfactory capabilities in detection and rescue dogs are well-known. However, the olfactory performance varies by breed and search environment (Jezierski et al. in Forensic Sci Int 237:112-118, 2014), as well as by the quantity of training (Horowitz et al. in Learn Motivation 44(4):207-217, 2013). While detection of an olfactory cue inherently demands a judgment regarding the presence or absence of a cue at a given location, olfactory discrimination requires an assessment of quantity, a task demanding more attention and, hence, decreasing reliability as an informational source (Horowitz et al. 2013). This study aims at gaining more clarity on detection and discrimination of olfactory cues in untrained dogs and in a variety of dog breeds. Using a two-alternative forced choice (2AFC) paradigm, we assessed olfactory detection scores by presenting a varied quantity of food reward under one or the other hidden cup, and discrimination scores by presenting two varied quantities of food reward under both hidden cups. We found relatively reliable detection performances across all breeds and limited discrimination abilities, modulated by breed. We discuss our findings in relation to the cognitive demands imposed by the tasks and the cephalic index of the dog breeds.

A machine learning approach to infant distress calls and maternal behaviour of wild chimpanzees.

Distress calls are an acoustically variable group of vocalizations ubiquitous in mammals and other animals. Their presumed function is to recruit help, but there has been much debate on whether the nature of the disturbance can be inferred from the acoustics of distress calls. We used machine learning to analyse episodes of distress calls of wild infant chimpanzees. We extracted exemplars from those distress call episodes and examined them in relation to the external event triggering them and the distance to the mother. In further steps, we tested whether the acoustic variants were associated with particular maternal responses. Our results suggest that, although infant chimpanzee distress calls are highly graded, they can convey information about discrete problems experienced by the infant and about distance to the mother, which in turn may help guide maternal parenting decisions. The extent to which mothers rely on acoustic cues alone (versus integrate other contextual-visual information) to decide upon intervening should be the focus of future research.

An information-theory approach to geometry for animal groups.

One of the hardest problems in studying animal behaviour is to quantify patterns of social interaction at the group level. Recent technological developments in global positioning system (GPS) devices have opened up new avenues for locating animals with unprecedented spatial and temporal resolution. Likewise, advances in computing power have enabled new levels of data analyses with complex mathematical models to address unresolved problems in animal behaviour, such as the nature of group geometry and the impact of group-level interactions on individuals. Here, we present an information theory-based tool for the analysis of group behaviour. We illustrate its affordances with GPS data collected from a freely interacting pack of 15 Siberian huskies (Canis lupus familiaris). We found that individual freedom in movement decisions was limited to about 4%, while a subject's location could be predicted with 96% median accuracy by the locations of other group members. Dominant individuals were less affected by other individuals' locations than subordinate ones, and same-sex individuals influenced each other more strongly than opposite-sex individuals. We also found that kinship relationships increased the mutual dependencies of individuals. Moreover, the network stability of the pack deteriorated with an upcoming feeding event. Together, we conclude that information theory-based approaches, coupled with state-of-the-art bio-logging technology, provide a powerful tool for future studies of animal social interactions beyond the dyadic level.

Social information in equine movement gestalts.

One model of signal evolution is based on the notion that behaviours become increasingly detached from their original biological functions to obtain a communicative value. Selection may not always favour the evolution of such transitions, for instance, if signalling is costly due to predators usurping signal production. Here, we collected inertial movement sensing data recorded from multiple locations in free-ranging horses (Equus caballus), which we subjected to a machine learning algorithm to extract kinematic gestalt profiles. This yielded surprisingly rich and multi-layered sets of information. In particular, we were able to discriminate identity, breed, sex and some personality traits from the overall movement patterns of freely moving subjects. Our study suggests that, by attending to movement gestalts, domestic horses, and probably many other group-living animals, have access to rich social information passively but reliably made available by conspecifics, a finding that we discuss in relation with current signal evolution theories.

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.

Rationality and cognitive bias in captive gorillas' and orang-utans' economic decision-making.

Human economic decision-making sometimes appears to be irrational. Partly, this is due to cognitive biases that can lead to suboptimal economic choices and context-dependent risk-preferences. A pertinent question is whether such biases are part of our evolutionary heritage or whether they are culturally acquired. To address this, we tested gorillas (Gorilla gorilla gorilla) and orang-utans (Pongo abelii) with two risk-assessment experiments that differed in how risk was presented. For both experiments, we found that subjects increased their preferences for the risky options as their expected gains increased, showing basic understanding of reward contingencies and rational decision-making. However, we also found consistent differences in risk proneness between the two experiments, as subjects were risk-neutral in one experiment and risk-prone in the other. We concluded that gorillas and orang-utans are economically rational but that their decisions can interact with pre-existing cognitive biases which modulates their risk-preference in context-dependent ways, explaining the variability of their risk-preference in previous literature.

Spatial organization of multisensory responses in temporal association cortex.

Neurons in sensory cortices are often topographically organized according to their response preferences. We here show that such an organization of response preferences also exists in multisensory association cortex. Using electrophysiological mappings, we probed the modality preference to auditory and visual stimuli of neurons in the superior temporal association cortex of nonhuman primates. We found that neurons preferring the same modality (auditory or visual) often co-occur in close spatial proximity or occur intermingled with bimodal neurons. Neurons preferring different modalities, in contrast, occur spatially separated. This organization at the scale of individual neurons leads to extended patches of same modality preference when analyzed at the scale of millimeters, revealing larger-scale regions that preferentially respond to the same modality. In addition, we find that neurons exhibiting signs of multisensory interactions, such as superadditive or subadditive response summation, also occur in spatial clusters. Together, these results reveal a spatial organization of modality preferences in a higher association cortex and lend support to the notion that topographical organizations might serve as a general principle of integrating information within and across the sensory modalities.

The Thatcher illusion in humans and monkeys.

Primates possess the remarkable ability to differentiate faces of group members and to extract relevant information about the individual directly from the face. Recognition of conspecific faces is achieved by means of holistic processing, i.e. the processing of the face as an unparsed, perceptual whole, rather than as the collection of independent features (part-based processing). The most striking example of holistic processing is the Thatcher illusion. Local changes in facial features are hardly noticeable when the whole face is inverted (rotated 180 degrees ), but strikingly grotesque when the face is upright. This effect can be explained by a lack of processing capabilities for locally rotated facial features when the face is turned upside down. Recently, a Thatcher illusion was described in the macaque monkey analogous to that known from human investigations. Using a habituation paradigm combined with eye tracking, we address the critical follow-up questions raised in the aforementioned study to show the Thatcher illusion as a function of the observer's species (humans and macaques), the stimulus' species (humans and macaques) and the level of perceptual expertise (novice, expert).

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.

Individuation and holistic processing of faces in rhesus monkeys.

Despite considerable evidence that neural activity in monkeys reflects various aspects of face perception, relatively little is known about monkeys' face processing abilities. Two characteristics of face processing observed in humans are a subordinate-level entry point, here, the default recognition of faces at the subordinate, rather than basic, level of categorization, and holistic effects, i.e. perception of facial displays as an integrated whole. The present study used an adaptation paradigm to test whether untrained rhesus macaques (Macaca mulatta) display these hallmarks of face processing. In experiments 1 and 2, macaques showed greater rebound from adaptation to conspecific faces than to other animals at the individual or subordinate level. In experiment 3, exchanging only the bottom half of a monkey face produced greater rebound in aligned than in misaligned composites, indicating that for normal, aligned faces, the new bottom half may have influenced the perception of the whole face. Scan path analysis supported this assertion: during rebound, fixation to the unchanged eye region was renewed, but only for aligned stimuli. These experiments show that macaques naturally display the distinguishing characteristics of face processing seen in humans and provide the first clear demonstration that holistic information guides scan paths for conspecific faces.

The nature and distribution of affiliative behaviour during exposure to mild threat.

Individual reactions to danger in humans are often characterized as antisocial and self-preservative. Yet, more than 50 years of research have shown that humans often seek social partners and behave prosocially when confronted by danger. This research has relied on post hoc verbal reports, which fall short of capturing the more spontaneous reactions to danger and determine their social nature. Real-world responses to danger are difficult to observe, due to their evanescent nature. Here, we took advantage of a series of photographs freely accessible online and provided by a haunted house attraction, which enabled us to examine the more immediate reactions to mild threat. Regarding the nature and structure of affiliative behaviour and their motivational correlates, we were able to analyse the distribution of gripping, a behaviour that could either be linked to self- or other-oriented protection. We found that gripping, an affiliative behaviour, was common, suggestive of the social nature of human immediate reactions to danger. We also found that, while gripping behaviour is quite stable across group sizes, mutual gripping dropped dramatically as group size increases. The fact that mutual gripping disappears when the number of available partners increases suggests that gripping behaviour most probably reflects a self-preservative motivation. We also found age class differences, with younger individuals showing more gripping but receiving little reciprocation. Also, the most exposed individuals received little mutual gripping. Altogether, these results suggest that primary reactions to threat in humans are driven by affiliative tendencies serving self-preservative motives.

Skin temperature changes in wild chimpanzees upon hearing vocalizations of conspecifics.

A growing trend of research using infrared thermography (IRT) has shown that changes in skin temperature, associated with activity of the autonomic nervous system, can be reliably detected in human and non-human animals. A contact-free method, IRT provides the opportunity to uncover emotional states in free-ranging animals during social interactions. Here, we measured nose and ear temperatures of wild chimpanzees of Budongo Forest, Uganda, when exposed to naturally occurring vocalizations of conspecifics. We found a significant temperature decrease over the nose after exposure to conspecifics' vocalizations, whereas we found a corresponding increase for ear temperature. Our study suggests that IRT can be used in wild animals to quantify changes in emotional states in response to the diversity of vocalizations, their functional significance and acoustical characteristics. We hope that it will contribute to more research on physiological changes associated with social interactions in wild animals.

Sequential information in a great ape utterance.

Birdsong is a prime example of acoustically sophisticated vocal behaviour, but its complexity has evolved mainly through sexual selection to attract mates and repel sexual rivals. In contrast, non-human primate calls often mediate complex social interactions, but are generally regarded as acoustically simple. Here, we examine arguably the most complex call in great ape vocal communication, the chimpanzee (Pan troglodytes schweinfurthii) 'pant hoot'. This signal consists of four acoustically distinct phases: introduction, build-up, climax and let-down. We applied state-of-the-art Support Vector Machines (SVM) methodology to pant hoots produced by wild male chimpanzees of Budongo Forest, Uganda. We found that caller identity was apparent in all four phases, but most strongly in the low-amplitude introduction and high-amplitude climax phases. Age was mainly correlated with the low-amplitude introduction and build-up phases, dominance rank (i.e. social status) with the high-amplitude climax phase, and context (reflecting activity of the caller) with the low-amplitude let-down phase. We conclude that the complex acoustic structure of chimpanzee pant hoots is linked to a range of socially relevant information in the different phases of the call, reflecting the complex nature of chimpanzee social lives.

Integration or separation in the processing of facial properties--a computational view.

A face recognition system ought to read out information about the identity, facial expression and invariant properties of faces, such as sex and race. A current debate is whether separate neural units in the brain deal with these face properties individually or whether a single neural unit processes in parallel all aspects of faces. While the focus of studies has been directed toward the processing of identity and facial expression, little research exists on the processing of invariant aspects of faces. In a theoretical framework we tested whether a system can deal with identity in combination with sex, race or facial expression using the same underlying mechanism. We used dimension reduction to describe how the representational face space organizes face properties when trained on different aspects of faces. When trained to learn identities, the system not only successfully recognized identities, but also was immediately able to classify sex and race, suggesting that no additional system for the processing of invariant properties is needed. However, training on identity was insufficient for the recognition of facial expressions and vice versa. We provide a theoretical approach on the interconnection of invariant facial properties and the separation of variant and invariant facial properties.

Own-race and own-species advantages in face perception: a computational view.

The frequency to which an organism is exposed to a particular type of face influences recognition performance. For example, Asians are better in individuating Asian than Caucasian faces, known as the own-race advantage. Similarly, humans in general are better in individuating human than monkey faces, known as the own-species advantage. It is an open question whether the underlying mechanisms causing these effects are similar. We hypothesize that these processes are governed by neural plasticity of the face discrimination system to retain optimal discrimination performance in its environment. Using common face features derived from a set of images from various face classes, we show that maximizing the feature variance between different individuals while ensuring minimal variance within individuals achieved good discrimination performances on own-class faces when selecting a subset of feature dimensions. Further, the selected subset of features does not necessarily lead to an optimal performance on the other class of faces. Thus, the face discrimination system continuously re-optimizes its space constraint face representation to optimize recognition performance on the current distribution of faces in its environment. This model can account for both, the own-race and own-species advantages. We name this approach Space Constraint Optimized Representational Embedding (SCORE).

The other-race and other-species effects in face perception - a subordinate-level analysis.

The ability of face discrimination is modulated by the frequency of exposure to a category of faces. In other words, lower discrimination performance was measured for infrequently encountered faces as opposed to frequently encountered ones. This phenomenon has been described in the literature: the own-race advantage, a benefit in processing own-race as opposed to the other-race faces, and the own-species advantage, a benefit in processing the conspecific type of faces as opposed to the heterospecific type. So far, the exact parameters that drive either of these two effects are not fully understood. In the following we present a full assessment of data in human participants describing the discrimination performances across two races (Asian and Caucasian) as well as a range of non-human primate faces (chimpanzee, Rhesus macaque and marmoset). We measured reaction times of Asian participants performing a delayed matching-to-sample task, and correlated the results with similarity estimates of facial configuration and face parts. We found faster discrimination of own-race above other-race/species faces. Further, we found a strong reliance on configural information in upright own-species/-race faces and on individual face parts in all inverted face classes, supporting the assumption of specialized processing for the face class of most frequent exposure.

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.

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.

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.

Second-order relational manipulations affect both humans and monkeys.

Recognition and individuation of conspecifics by their face is essential for primate social cognition. This ability is driven by a mechanism that integrates the appearance of facial features with subtle variations in their configuration (i.e., second-order relational properties) into a holistic representation. So far, there is little evidence of whether our evolutionary ancestors show sensitivity to featural spatial relations and hence holistic processing of faces as shown in humans. Here, we directly compared macaques with humans in their sensitivity to configurally altered faces in upright and inverted orientations using a habituation paradigm and eye tracking technologies. In addition, we tested for differences in processing of conspecific faces (human faces for humans, macaque faces for macaques) and non-conspecific faces, addressing aspects of perceptual expertise. In both species, we found sensitivity to second-order relational properties for conspecific (expert) faces, when presented in upright, not in inverted, orientation. This shows that macaques possess the requirements for holistic processing, and thus show similar face processing to that of humans.