Human Attentional State Research Articles

Bottlenose dolphins are sensitive to human attentional features, including eye functionality

The ability to attribute attentional states to other individuals is a highly adaptive socio-cognitive skill and thus may have evolved in many social species. However, whilst humans excel in this ability, even chimpanzees appear to not accurately understand how visual attention works, particularly in regard to the function of eyes. The complex socio-ecological background and socio-cognitive skill-set of bottlenose dolphins (Tursiops sp.), alongside the specialised training that captive dolphins typically undergo, make them an especially relevant candidate for an investigation into their sensitivity to human attentional states. Therefore, we tested 8 bottlenose dolphins on an object retrieval task. The dolphins were instructed to fetch an object by a trainer under various attentional state conditions involving the trainer’s eyes and face orientation: ‘not looking’, ‘half looking’, ‘eyes open’, and ‘eyes closed’. As the dolphins showed an increased latency to retrieve the object in conditions where the trainer’s head and eyes cued a lack of attention to the dolphin, particularly when comparing ‘eyes open’ vs ‘eyes closed’ conditions, we demonstrate that dolphins can be sensitive to human attentional features, namely the functionality of eyes. This study supports growing evidence that dolphins possess highly complex cognitive abilities, particularly those in the social domain.

Eye-Fixation-Related Potentials (EFRPs) As a Predictor of Human Error Occurrences During a Visual Inspection Task.

Estimation of human attentional states using an electroencephalogram (EEG) has been demonstrated to help prevent human errors associated with the degradation. Since the use of the lambda response -one of eye-fixation-related potentials time-locked to the saccade offset- enables such estimation without external triggers, the measurements are compatible for an application in a real-world environment. With aiming to apply the lambda response as an index of human errors during the visual inspection, the current research elucidated whether the mean amplitude of the lambda response was a predictor of the number of inspection errors. EEGs were measured from 50 participants while inspecting the differences between two images of the circuit board. Twenty percent of the total number of image pairs included differences. The lambda response was obtained relative to a saccade offset starting a fixation of the inspection image. Participants conducted four sessions over two days (625 trials/ session, 2 sessions/ day). A Poisson regression of the number of inspection errors using a generalized linear mixed model showed that a coefficient of the mean amplitude of the lambda response was significant , suggesting that the response has a role in th$(\hat \beta = 0.24,p < 0.01)$e prediction of the number of human error occurrences in the visual inspection.

Visual Attention Patterns Differ in Dog vs. Cat Interactions With Children With Typical Development or Autism Spectrum Disorders.

Visual social attention is an important part of the social life of many species, including humans, but its patterning may vary between species. Studies on human–pet relationships have revealed that visual attention is also part of such interspecific interactions and that pets are sensitive to the human visual attentional state. It has been argued that domestication and/or repeated experiences with humans have shaped and refined these decoding abilities. Little is known on how the species’ evolutionary history may play a role in determining visual attention patterns during interactions, nor how the human’s own social skills may influence the animal’s attention patterns in human–animal interactions. In the present study, we investigated the visual attention patterns directed to the partner in dog–child and cat–child interactions in their home environment. We also compared these patterns between a group of children with autism spectrum disorders (ASD) and children with typical development. We found that the attention patterns differed according to species, with dogs displaying more gazes and cats more glances toward their human interlocutor, while children showed gazes toward both species. Only slight differences were observed according to the developmental status of children: ASD children displayed much more visual attention with their pet cat than with their pet dog and the same amount of visual attention toward their pet, whatever the species, as typically developing (TD) children. Because humans rely a lot upon visual communication in their own social encounters, where direct gazes play a major role from early on, they may be especially sensitive to the gazing behavior of their dogs. People with ASD, with a less typical pattern of interaction, may be more comfortable with the less “invasive” short glances of cats. These results suggest not only that interspecific communication has to be associated with processing and storing the other species’ ways of communicating in order to be successful but also that visual attention patterns during interactions, even when interspecific, are, for a large part, the result of the species’ own evolutionary history.

Intrinsic Ball Retrieving in Wolf Puppies Suggests Standing Ancestral Variation for Human-Directed Play Behavior.

SummaryDomestication dramatically alters phenotypes across animal species. Standing variation among ancestral populations often drives phenotypic change during domestication, but some changes are caused by novel mutations. In dogs (Canis familiaris) specifically, it has been suggested that the ability to interpret social-communicative behavior expressed by humans originated post-domestication and this behavior is thus not expected to occur in wolves (Canis lupus). Here we report the observation of three 8-week-old wolf puppies spontaneously responding to social-communicative behaviors from an unfamiliar person by retrieving a ball. This behavioral expression in wolves has significant implications for our understanding and expectations of the genetic foundations of dog behavior. Importantly, our observations indicate that behavioral responses to human social-communicative cues are not unique to dogs. This suggests that, although probably rare, standing variation in the expression of human-directed behavior in ancestral populations could have been an important target for early selective pressures exerted during dog domestication.

The effects of human attentional state on canine gazing behaviour: a comparison of free-ranging, shelter, and pet dogs.

The ability of animals to communicate using gaze is a rich area of research. How domestic dogs (Canis lupus familiaris) use and respond to the gaze of humans is an area of particular interest. This study examined how three groups of domestic dogs from different populations (free-ranging dogs, pet dogs, and shelter dogs) responded to a human during three attentional state conditions: when the human was making eye contact (attentive), when the human was turned away (inattentive), and when the human exited the testing area. We found that dogs from different populations differed in their gazing behaviour. Free-ranging dogs responded to the human's change in attentional state by looking significantly less at the human in the inattentive condition compared to the attentive condition. Pet and shelter dogs did not differ in their gazing behaviour between these conditions. However, they gazed significantly more at the human in both the inattentive and attentive conditions compared to the free-ranging dogs and also spent more time in the proximity of the experimenter. This study suggests that life experience plays an important role in how dogs respond to the attentional state of a human.

The quality of being sociable: The influence of human attentional state, population, and human familiarity on domestic cat sociability

Two experiments were conducted to assess the influence of human attentional state, population, and human familiarity on domestic cat sociability. Sociability behaviors included duration of time in proximity and contact with the human and the frequency of meow vocalizations. Human attentional state influenced cat behavior, with cats spending significantly more time in proximity with the attentive human in both the pet (U(22) = 389, Z = -2.72, P = 0.007) and shelter groups (F(44) = 15.34, P = 0.0003). Cat population influenced sociability and shelter cats spent more time in proximity with the inattentive unfamiliar human as compared to pet cats (U(44) = 91, Z = 3.8, P = 0.0001) Additionally compared to pet cats, more individuals in the shelter cat group meowed at least once during the unfamiliar human inattentive phase (Fisher’s exact test, P = 0.02). Human familiarity did not significantly influence pet cat sociability behaviors. Overall, a wide range of sociability scores was seen, indicating individual variation is an important consideration in cat social behavior. Future research in this area will predict conditions under which strong cat-human bonds form and establish a more comprehensive scientific understanding of cat behavior.

Intentional gestural communication and discrimination of human attentional states in rhesus macaques (Macaca mulatta).

The present study tested intentionality of a learned begging gesture and attention-reading abilities in rhesus macaques (Macaca mulatta). Subjects were trained to produce a begging gesture towards a hidden food reward that could be delivered by a human experimenter. More specifically, we investigated which attentional cues--body, face and/or eyes orientation of a human partner--were taken into account by the macaques in order to communicate with her. Our results provide strong evidence of intentional communication: the monkeys adjusted their behaviour to that of the partner. The latter's attentional state influenced the monkeys' likelihood of performing begging gestures and showing gaze alternation between the partner and the hidden food. By contrast, we found no evidence of attention-getting behaviours, persistence or elaboration of new communicative behaviours. Our results also showed that rhesus macaques discriminated gross cues including the presence, body and face orientation of the human experimenter but not her eyes. However, the monkeys emitted more gaze alternation and monitored the human's attentional state more closely when she also displayed gaze alternation, suggesting an important role of joint attention in gestural communication.

Tufted capuchins (Cebus apella) adapt their communicative behaviour to human's attentional states.

Animal communication has become a widely studied field of research, especially because of the associated debates on the origin of human language. Due to their phylogenetic proximity with humans, non-human primates represent a suitable model to investigate the precursors of language. This study focuses on the perception of the attentional states of others, an important prerequisite to intentional communication. We investigated whether capuchins (Cebus apella) produce a learnt pointing gesture towards a hidden and unreachable food reward as a function of the attentional status of the human experimenter. For that purpose, we tested five subjects that we first trained to indicate by a pointing gesture towards the human partner the position of a reward hidden by an assistant. Then, capuchins were tested in two experimental conditions randomly ordered. In the first condition-motivation trial-the experimenter was attentive to the subject gestures and rewarded him immediately when it pointed towards the baited cylinder. During the second condition-test trial-the experimenter adopted one of the following attention states and the subject was rewarded after 10 s has elapsed, regardless of the subject's behaviour. Five attentional states were tested: (1) experimenter absent, (2) experimenter back to the monkey, (3) experimenter's head away, (4) experimenter watching above the monkey, and (5) experimenter watching the monkey face. Our results reveal a variation in our subjects' communicative behaviours with a discrimination of the different postural clues (body and head orientation) available in our experimental conditions. This study suggests that capuchins can flexibly use a communicative gesture to adapt to the attentional state of their partner and provides evidence that acquired communicative gestures of monkeys might be used intentionally.

Do Tonkean macaques (Macaca tonkeana) tailor their gestural and visual signals to fit the attentional states of a human partner?

We tested here whether Tonkean macaques (Macaca tonkeana), trained to produce a pointing gesture, modify their behaviour in response to different human's attentional states. More specifically, we investigated the macaque's ability to communicate intentionally about the location of an unreachable hidden food reward in several contexts which differ by the human partner's attentional state. The experimenter displayed seven attentional states differing on the basis of body, head and gaze orientation. Our study validates several criteria of an intentional communication. We showed that macaques produce more pointing gestures when an audience, i.e. the human partner, is present than absent. We also revealed an adjustment of gaze alternation between the face of the experimenter and the hidden food reward according to several experimental conditions. However, in our study, macaques did not produce auditory attention-getting behaviours when the human partner was inattentive. Finally, only rough cues, i.e. presence, body and face orientation of the observer, seem to be taken into account by macaques. However, our results also supposed the importance of joint attention for macaques since they display more gaze alternation when the head and/or eyes of the human partner are mobile.

To beg, or not to beg? That is the question: mangabeys modify their production of requesting gestures in response to human's attentional states.

BackgroundAlthough gestural communication is widespread in primates, few studies focused on the cognitive processes underlying gestures produced by monkeys.Methodology/Principal FindingsThe present study asked whether red-capped mangabeys (Cercocebus torquatus) trained to produce visually based requesting gestures modify their gestural behavior in response to human’s attentional states. The experimenter held a food item and displayed five different attentional states that differed on the basis of body, head and gaze orientation; mangabeys had to request food by extending an arm toward the food item (begging gesture). Mangabeys were sensitive, at least to some extent, to the human’s attentional state. They reacted to some postural cues of a human recipient: they gestured more and faster when both the body and the head of the experimenter were oriented toward them than when they were oriented away. However, they did not seem to use gaze cues to recognize an attentive human: monkeys begged at similar levels regardless of the experimenter’s eyes state.Conclusions/SignificanceThese results indicate that mangabeys lowered their production of begging gestures when these could not be perceived by the human who had to respond to it. This finding provides important evidence that acquired begging gestures of monkeys might be used intentionally.

Chimpanzees (Pan troglodytes) show more understanding of human attentional states when they request food in the experimenter’s hand than on the table

Although chimpanzees have been reported to understand to some extent others’ visual perception, previous studies using food requesting tasks are divided on whether or not chimpanzees understand the role of eye gaze. One plausible reason for this discrepancy may be the familiarity of the testing situation. Previous food requesting tasks with negative results used an unfamiliar situation that may be difficult for some chimpanzees to recognize as a requesting situation, whereas those with positive results used a familiar situation. The present study tested chimpanzees’ understanding of others’ attentional states by comparing two requesting situations: an unfamiliar situation in which food was put on a table, and a familiar situation in which chimpanzees requested food held by an experimenter. Chimpanzees showed evidence of understanding the experimenter’s attentional variations and the role of eye gaze only in the latter task. This suggests that an unfamiliar requesting situation may keep subjects from expressing their understanding of others’ attentional states even though they are sensitive to them. Keywords: Understanding attention; Social cognition; Chimpanzees

Reevaluating canine perspective-taking behavior

Udell, Dorey, and Wynne (2011) demonstrated that both domesticated and nondomesticated canids-specifically, gray wolves-have the capacity to succeed on perspective-taking tasks, suggesting that dogs' ability to respond to the human attentional state is not a by-product of domestication alone. Furthermore, not all dogs were successful on the task. Instead, the occluder type used was a strong predictor of performance, indicating the important role of environment and experience for tasks of this type. Here, we address several commentaries reflecting on the methods and design of that study, as well as the interpretation of the results. We also discuss the positive shift toward more interactive approaches in the field of canine behavior and cognition. Finally, we question the functionality of describing canine social behavior in terms of theory of mind.

Can your dog read your mind? Understanding the causes of canine perspective taking

Prior studies have documented the domestic dog's (Canis lupus familiaris) sensitivity to human attentional state, including a tendency to preferentially beg for food from attentive individuals and an ability to selectively perform forbidden behaviors when humans are not looking. Due to the success of dogs on perspective-taking tasks, some have hypothesized that domestic dogs may have theory of mind, or the ability to infer what other individuals know. Here we provide the first evidence that nondomesticated canids, grey wolves (Canis lupus), are also sensitive to human attentional state under some conditions. We also demonstrate that dogs do not display an undifferentiated sensitivity to all visual cues of attentional state. Rather, dogs are more sensitive to stimuli encountered in their home environment. Some dogs perform poorly on perspective-taking tasks. These findings have important implications for the interpretation of research designed to understand complex social cognition across species.

Focus on the essential: all great apes know when others are being attentive

When begging for food, all great ape species are sensitive to a human's attention. However, studies investigating which cues are relevant for chimpanzees to assess the attentional state of others have produced highly inconsistent results. Some have suggested chimpanzees differentiate attention based on the status of the face or even the eyes, while others have indicated that body posture alone is the relevant cue. Kaminski et al. (Anim Cogn 7:216-223, 2004) compared the behaviour of chimpanzees, bonobos and orangutans while begging for food from a human experimenter who systematically varied his face and body orientation. Their results indicated that both factors, face and body orientation, affect apes' begging behaviour. The authors claimed that while body orientation provides information about the experimenter's general disposition to offer food, the visibility of the face provides information about the human's attentional state. In the current study, we tested this hypothesis with all four great apes species. However, unlike Kaminski et al. (Anim Cogn 7:216-223, 2004), the experimenter was able to hand over food regardless of body orientation. The results show that as soon as the offering of the food was no longer restricted, the orientation of the face became the key factor. Therefore, we present the first evidence that all great ape species are able to assess the attentional state of a recipient based on the orientation of the face.

What did domestication do to dogs? A new account of dogs' sensitivity to human actions

Over the last two decades increasing evidence for an acute sensitivity to human gestures and attentional states in domestic dogs has led to a burgeoning of research into the social cognition of this highly familiar yet previously under-studied animal. Dogs (Canis lupus familiaris) have been shown to be more successful than their closest relative (and wild progenitor) the wolf, and than man's closest relative, the chimpanzee, on tests of sensitivity to human social cues, such as following points to a container holding hidden food. The "Domestication Hypothesis" asserts that during domestication dogs evolved an inherent sensitivity to human gestures that their non-domesticated counterparts do not share. According to this view, sensitivity to human cues is present in dogs at an early age and shows little evidence of acquisition during ontogeny. A closer look at the findings of research on canine domestication, socialization, and conditioning, brings the assumptions of this hypothesis into question. We propose the Two Stage Hypothesis, according to which the sensitivity of an individual animal to human actions depends on acceptance of humans as social companions, and conditioning to follow human limbs. This offers a more parsimonious explanation for the domestic dog's sensitivity to human gestures, without requiring the use of additional mechanisms. We outline how tests of this new hypothesis open directions for future study that offer promise of a deeper understanding of mankind's oldest companion.

Tufted capuchin monkeys (Cebus apella) show understanding of human attentional states when requesting food held by a human

Researchers have investigated to what extent non-human primates understand others' attentional states, as this ability is considered an important prerequisite for theory of mind. However, previous studies using food requesting tasks have failed to show that non-human primates attribute perception to others as a function of their attentional states. One possible reason is that food requesting tasks may require subjects not only to take into account an experimenter's attentional state but also to direct it toward the food. The present study tested tufted capuchin monkeys' (Cebus apella) understanding of others' attentional states in a food requesting task. In the first situation, monkeys were required only to attract an experimenter's attention. In the second situation, the monkeys were required to both attract the experimenter's attention and direct it toward food on a table. The results revealed that capuchin monkeys showed evidence of understanding the experimenter's attentional variations only in the former condition. This suggests that previous tasks, requiring referential gestures, lacking in most non-human primates, failed to reveal sensitivity to human attentional states because the subjects might not have understood the requesting situation. In conclusion, capuchin monkeys can understand variations in others' attentional states, although this ability appears limited compared to what is seen in humans.

Jackdaws Respond to Human Attentional States and Communicative Cues in Different Contexts

Humans communicate their intentions and disposition using their eyes, whereas the communicative function of eyes in animals is less clear. Many species show aversive reactions to eyes, and several species gain information from conspecifics' gaze direction by automatically co-orienting with them. However, most species show little sensitivity to more subtle indicators of attention than head orientation and have difficulties using such cues in a cooperative context. Recently, some species have been found responsive to gaze direction in competitive situations. We investigated the sensitivity of jackdaws, pair-bonded social corvids that exhibit an analogous eye morphology to humans, to subtle attentional and communicative cues in two contexts and paradigms. In a conflict paradigm, we measured the birds' latency to retrieve food in front of an unfamiliar or familiar human, depending on the state and orientation of their eyes toward food. In a cooperative paradigm, we tested whether the jackdaws used familiar human's attentional or communicative cues to locate hidden food. Jackdaws were sensitive to human attentional states in the conflict situation but only responded to communicative cues in the cooperative situation. These findings may be the result of a natural tendency to attend to conspecifics' eyes or the effect of intense human contact during socialization.

Dog-Human communication through a keyboard: Is human attentional state relevant?

Dog-Human communication through a keyboard: Is human attentional state relevant?

I know you are not looking at me: capuchin monkeys’ (Cebus apella) sensitivity to human attentional states

The present study asked whether capuchin monkeys recognize human attentional states. The monkeys requested food from the experimenter by extending an arm (pointing) toward the baited one of two transparent cups. On regular trials the experimenter gave the food immediately to the monkeys upon pointing but on randomly inserted test trials she ignored the pointing for 5 s during which she displayed different attentional states. The monkeys looked at the experimenter's face longer when she looked at the monkeys than when she looked at the ceiling in Experiment 1, and longer when she oriented her head midway between the two cups with eyes open than when she did so with eyes closed in Experiment 2. However, the monkeys showed no differential pointing in these conditions. These results suggest that capuchins are sensitive to eye direction but this sensitivity does not lead to differential pointing trained in laboratory experiments. Furthermore, to our knowledge, this is the first firm behavioral evidence that non-human primates attend to the subtle states of eyes in a food requesting task.