Crucial information for efficient face searching by humans and Japanese macaques

Humans can efficiently detect a face among non-face objects, but few studies of this ability have been conducted in animals. Here, in Japanese macaques and humans, we examined visual searching for a face and explored what factors contribute to efficient facial information processing. Subjects were asked to search for an odd target among the different numbers of distracters. Faces of the subjects’ own species, the backs of the head of the subjects’ own species, faces of the subjects’ closely related species or race, and faces of species that are clearly different from the subjects’ own species were used as the target. Both the macaques and humans detected a face of their own species more efficiently than a face from a clearly different species. Similar efficient detections were confirmed for the faces of the subjects’ closely related species or race. These results suggest that conspecific faces and faces that share morphological similarity with conspecific faces can be detected efficiently among non-face objects by both humans and Japanese macaques. In another experiment, facial recognition efficiency was observed when the subjects searched for own-species faces that had lower-spatial-frequency components compared to faces with higher-spatial-frequency components. It seems reasonable that the ability to search efficiently for faces by using holistic face processing is derived from fundamental social cognition abilities that are broadly shared among species.     

Parasitic egg rejection decisions of chalk-browed mockingbirds <Emphasis Type="Italic">Mimus saturninus</Emphasis> are independent of clutch composition

Obligate avian brood parasites lay their eggs in nests of other host species, which assume all the costs of parental care for the foreign eggs and chicks. The most common defensive response to parasitism is the rejection of foreign eggs by hosts. Different cognitive mechanisms and decision-making rules may guide both egg recognition and rejection behaviors. Classical optimization models generally assume that decisions are based on the absolute properties of the options (i.e., absolute valuation). Increasing evidence shows instead that hosts’ rejection decisions also depend on the context in which options are presented (i.e., context-dependent valuation). Here we study whether the chalk-browed mockingbird’s (Mimus saturninus) rejection of parasitic shiny cowbird (Molothrus bonariensis) eggs is a fixed behavior or varies with the context of the clutch. We tested three possible context-dependent mechanisms: (1) range effect, (2) habituation to variation, and (3) sensitization to variation. We found that mockingbird rejection of parasitic eggs does not change according to the characteristics of the other eggs in the nest. Thus, rejection decisions may exclusively depend on the objective characteristics of the eggs, meaning that the threshold of acceptance or rejection of a foreign egg is context-independent in this system.     

Anuran predators overcome visual illusion: dazzle coloration does not protect moving prey

Predators everywhere impose strong selection pressures on the morphology and behavior of their prey, but the resulting antipredator adaptations vary greatly among species. Studies of adaptive coloration in prey species have generally focused on cryptic or aposematic prey, with little consideration of color patterns in palatable mobile prey. Complex color patterns have been proposed to decrease the ability of visual predators to capture moving prey (motion dazzle effect). Most support for this hypothesis, however, comes from experiments with human subjects and simulated prey. We tested the motion dazzle effect using, for the first time, natural predators (cane toads, Rhinella marina) and live prey (house crickets, Acheta domesticus) with altered color patterns. We found no support for the motion dazzle effect as striped crickets did not fare better than solid colored ones. Crickets that spent more time moving, however, were more likely to be eaten. Our results suggest that motion specialized visual predators such as toads overcome the motion dazzle effect and impose stronger selection pressure on prey behavior than on coloration. These findings emphasize the importance of sensory specializations of predators in mediating antipredator strategies.     

The effect of experience and of dots’ density and duration on the detection of coherent motion in dogs

Knowledge about the mechanisms underlying canine vision is far from being exhaustive, especially that concerning post-retinal elaboration. One aspect that has received little attention is motion perception, and in spite of the common belief that dogs are extremely apt at detecting moving stimuli, there is no scientific support for such an assumption. In fact, we recently showed that dogs have higher thresholds than humans for coherent motion detection (Kanizsar et al. in Sci Rep UK 7:11259, 2017). This term refers to the ability of the visual system to perceive several units moving in the same direction, as one coherently moving global unit. Coherent motion perception is commonly investigated using random dot displays, containing variable proportions of coherently moving dots. Here, we investigated the relative contribution of local and global integration mechanisms for coherent motion perception, and changes in detection thresholds as a result of repeated exposure to the experimental stimuli. Dogs who had been involved in the previous study were given a conditioned discrimination task, in which we systematically manipulated dot density and duration and, eventually, re-assessed our subjects’ threshold after extensive exposure to the stimuli. Decreasing dot duration impacted on dogs’ accuracy in detecting coherent motion only at very low duration values, revealing the efficacy of local integration mechanisms. Density impacted on dogs’ accuracy in a linear fashion, indicating less efficient global integration. There was limited evidence of improvement in the re-assessment but, with an average threshold at re-assessment of 29%, dogs’ ability to detect coherent motion remains much poorer than that of humans.     

The eyes have it: lateralized coping strategies in cattle herds responding to human approach

We report a range of lateralized coping strategies adopted by large social groups of cattle in response to mild challenges posed by humans of varying degrees of familiarity. At either 14 or 18 pens at a commercial feedlot, with 90 to 200 cattle in each, we conducted a series of video recorded ‘pressure tests’. ‘Frontal’ pressure tests involved walking from a position perpendicular to the concrete feed bunk of a given pen, towards the geometric centre of the line of feeding cattle. ‘Bunk-side’ pressure tests involved experimenters walking closely past a pen of feeding cattle in one direction, before returning in the opposite direction shortly afterwards. Experimenters wore white dust masks to alter their facial features in the bunk-side pressure tests. In both frontal and bunk-side pressure tests, distance from the experimenter influenced cattle’s choice of binocular viewing, cessation of feeding, standing or stepping backwards to monitor the approach and leaving the feed bunk. The frequency of these coping strategies differed in a lateralized manner. The cattle were more likely to accept the close positioning of a generally familiar, unmasked human on their left, which is traditionally referred to as the “near” side. By contrast, when responding to the approach of an unfamiliar, masked human, cattle conformed to the general vertebrate model and were more likely to remove themselves from the potential threat viewed within the left and not right visual field. We argue that the traditional terms for livestock sidedness as “near” (left) and “off” (right) sides demonstrate a knowledge of behavioural lateralization in domestic livestock that has existed for over 300 years of stock handling.     

Individual identity and affective valence in marmoset calls: in vivo brain imaging with vocal sound playback

As with humans, vocal communication is an important social tool for nonhuman primates. Common marmosets (Callithrix jacchus) often produce whistle-like ‘phee’ calls when they are visually separated from conspecifics. The neural processes specific to phee call perception, however, are largely unknown, despite the possibility that these processes involve social information. Here, we examined behavioral and whole-brain mapping evidence regarding the detection of individual conspecific phee calls using an audio playback procedure. Phee calls evoked sound exploratory responses when the caller changed, indicating that marmosets can discriminate between caller identities. Positron emission tomography with [¹⁸F] fluorodeoxyglucose revealed that perception of phee calls from a single subject was associated with activity in the dorsolateral prefrontal, medial prefrontal, orbitofrontal cortices, and the amygdala. These findings suggest that these regions are implicated in cognitive and affective processing of salient social information. However, phee calls from multiple subjects induced brain activation in only some of these regions, such as the dorsolateral prefrontal cortex. We also found distinctive brain deactivation and functional connectivity associated with phee call perception depending on the caller change. According to changes in pupillary size, phee calls from a single subject induced a higher arousal level compared with those from multiple subjects. These results suggest that marmoset phee calls convey information about individual identity and affective valence depending on the consistency or variability of the caller. Based on the flexible perception of the call based on individual recognition, humans and marmosets may share some neural mechanisms underlying conspecific vocal perception.     

Tool-use training temporarily enhances cognitive performance in long-tailed macaques (<Emphasis Type="Italic">Macaca fascicularis</Emphasis>)

Tool use relies on numerous cognitive functions, including sustained attention and understanding of causality. In this study, we investigated the effects of tool-use training on cognitive performance in primates. Specifically, we applied the Primate Cognition Test Battery to three long-tailed macaques (Macaca fascicularis) at different stages of a training procedure that consisted of using a rake to retrieve out-of-reach food items. In addition, we evaluated a control group (n?=?3) performing a grasping task, in order to account for possible effects related to a simple motor act. Our results showed that tool-use training enhances mean performance in the physical cognition domain, i.e. the understanding of spatial relations, numerosity and causality. In particular, causal cognition (evaluating noise- and shape-related causality and understanding of tool properties) showed significant improvement after training, whereas spatial cognition (evaluating spatial memory, object permanence, rotation and transposition) showed a trend to improvement. Despite these findings, none of our trained monkeys succeeded in the tool-use task of the Primate Cognition Test Battery, which involved an unfamiliar tool. Some training-related effects did not persist after a 35-day resting period, suggesting that continuous practice may be necessary, or that a longer training period before resting may be needed to better maintain cognitive performance. In contrast with the training group, the control group did not display any change in cognitive performance. This finding paves the way to further investigation into the link between tool-use behaviour and the evolution of primate cognition.     

Spatial representation of magnitude in humans (<Emphasis Type="Italic">Homo sapiens</Emphasis>), Western lowland gorillas (<Emphasis Type="Italic">Gorilla gorilla gorilla</Emphasis>), and American black bears (<Emphasis Type="Italic">Ursus americanus</Emphasis>)

The spatial-numerical association of response codes (SNARC) effect is the tendency for humans to respond faster to relatively larger numbers on the left or right (or with the left or right hand) and faster to relatively smaller numbers on the other side. This effect seems to occur due to a spatial representation of magnitude either in occurrence with a number line (wherein participants respond to relatively larger numbers faster on the right), other representations such as clock faces (responses are reversed from number lines), or culturally specific reading directions, begging the question as to whether the effect may be limited to humans. Given that a SNARC effect has emerged via a quantity judgement task in Western lowland gorillas and orangutans (Gazes et al., Cog 168:312–319, 2017), we examined patterns of response on a quantity discrimination task in American black bears, Western lowland gorillas, and humans for evidence of a SNARC effect. We found limited evidence for SNARC effect in American black bears and Western lowland gorillas. Furthermore, humans were inconsistent in direction and strength of effects, emphasizing the importance of standardizing methodology and analyses when comparing SNARC effects between species. These data reveal the importance of collecting data with humans in analogous procedures when testing nonhumans for effects assumed to bepresent in humans.     

Interspecies transmission of emotional information via chemosignals: from humans to dogs (<Emphasis Type="Italic">Canis lupus familiaris</Emphasis>)

We report a study examining interspecies emotion transfer via body odors (chemosignals). Do human body odors (chemosignals) produced under emotional conditions of happiness and fear provide information that is detectable by pet dogs (Labrador and Golden retrievers)? The odor samples were collected from the axilla of male donors not involved in the main experiment. The experimental setup involved the co-presence of the dog’s owner, a stranger and the odor dispenser in a space where the dogs could move freely. There were three odor conditions [fear, happiness, and control (no sweat)] to which the dogs were assigned randomly. The dependent variables were the relevant behaviors of the dogs (e.g., approaching, interacting and gazing) directed to the three targets (owner, stranger, sweat dispenser) aside from the dogs’ stress and heart rate indicators. The results indicated with high accuracy that the dogs manifested the predicted behaviors in the three conditions. There were fewer and shorter owner directed behaviors and more stranger directed behaviors when they were in the “happy odor condition” compared to the fear odor and control conditions. In the fear odor condition, they displayed more stressful behaviors. The heart rate data in the control and happy conditions were significantly lower than in the fear condition. Our findings suggest that interspecies emotional communication is facilitated by chemosignals.