Development of gaze following abilities in wolves (Canis lupus)

The ability to coordinate with others' head and eye orientation to look in the same direction is considered a key step towards an understanding of others mental states like attention and intention. Here, we investigated the ontogeny and habituation patterns of gaze following into distant space and behind barriers in nine hand-raised wolves. We found that these wolves could use conspecific as well as human gaze cues even in the barrier task, which is thought to be more cognitively advanced than gazing into distant space. Moreover, while gaze following into distant space was already present at the age of 14 weeks and subjects did not habituate to repeated cues, gazing around a barrier developed considerably later and animals quickly habituated, supporting the hypothesis that different cognitive mechanisms may underlie the two gaze following modalities. More importantly, this study demonstrated that following another individuals' gaze around a barrier is not restricted to primates and corvids but is also present in canines, with remarkable between-group similarities in the ontogeny of this behaviour. This sheds new light on the evolutionary origins of and selective pressures on gaze following abilities as well as on the sensitivity of domestic dogs towards human communicative cues.     

Gaze direction - a cue for hidden food in rooks (Corvus frugilegus)?

Other individual's head- and eye-directions can be used as social cues indicating the presence of important events. Among birds, ravens and rooks have been shown to co-orient with conspecifics and with humans by following their gaze direction into distant space and behind visual screens. Both species use screens to cache food in private; also, it had been suggested that they may rely on gaze cues to detect hidden food. However, in an object-choice task, ravens failed to do so, and their competitive lifestyle may have prevented them from relying on these cues. Here we tested closely related and cooperative rooks. Food was hidden in one of two cups and the experimenter gazed at the baited cup. In a second experiment, we aimed to increase the birds’ motivation to choose correctly by increasing the investment needed to obtain the reward. To do so, the birds had to pull on a string to obtain the cup. Here, the birds as a group tended to rely on gaze cues. In addition, individual birds quickly learned to use the cue in both experiments. Although rooks may not use gaze cues to find hidden food spontaneously, they may quickly learn to do so.     

Influence of Turn-Taking in a Two-Person Conversation on the Gaze of a Viewer

In natural conversation, the minimal gaps and overlaps of the turns at talk indicate an accurate regulation of the timings of the turn-taking system. Here we studied how the turn-taking affects the gaze of a non-involved viewer of a two-person conversation. The subjects were presented with a video of a conversation while their eye gaze was tracked with an infrared camera. As a control, the video was presented without sound and the sound with still image of the speakers. Turns at talk directed the gaze behaviour of the viewers; the gaze followed, rather than predicted, the speakership change around the turn transition. Both visual and auditory cues presented alone also induced gaze shifts towards the speaking person, although significantly less and later than when the cues of both modalities were available. These results show that the organization of turn-taking has a strong influence on the gaze patterns of even non-involved viewers of the conversation, and that visual and auditory cues are in part redundant in guiding the viewers’ gaze.     

Ravens, Corvus corax, follow gaze direction of humans around obstacles

The ability to follow gaze (i.e. head and eye direction) has recently been shown for social mammals, particularly primates. In most studies, individuals could use gaze direction as a behavioural cue without understanding that the view of others may be different from their own. Here, we show that hand-raised ravens not only visually co-orient with the look-ups of a human experimenter but also reposition themselves to follow the experimenter's gaze around a visual barrier. Birds were capable of visual co-orientation already as fledglings but consistently tracked gaze direction behind obstacles not before six months of age. These results raise the possibility that sub-adult and adult ravens can project a line of sight for the other person into the distance. To what extent ravens may attribute mental significance to the visual behaviour of others is discussed.     

What We Observe Is Biased by What Other People Tell Us: Beliefs about the Reliability of Gaze Behavior Modulate Attentional Orienting to Gaze Cues

For effective social interactions with other people, information about the physical environment must be integrated with information about the interaction partner. In order to achieve this, processing of social information is guided by two components: a bottom-up mechanism reflexively triggered by stimulus-related information in the social scene and a top-down mechanism activated by task-related context information. In the present study, we investigated whether these components interact during attentional orienting to gaze direction. In particular, we examined whether the spatial specificity of gaze cueing is modulated by expectations about the reliability of gaze behavior. Expectations were either induced by instruction or could be derived from experience with displayed gaze behavior. Spatially specific cueing effects were observed with highly predictive gaze cues, but also when participants merely believed that actually non-predictive cues were highly predictive. Conversely, cueing effects for the whole gazed-at hemifield were observed with non-predictive gaze cues, and spatially specific cueing effects were attenuated when actually predictive gaze cues were believed to be non-predictive. This pattern indicates that (i) information about cue predictivity gained from sampling gaze behavior across social episodes can be incorporated in the attentional orienting to social cues, and that (ii) beliefs about gaze behavior modulate attentional orienting to gaze direction even when they contradict information available from social episodes.     

线索有效性对社会性注意和外源性注意的影响

目的 眼睛注视、头朝向和生物运动方向等社会性线索,对人类的生存和社会交互极为重要.由于社会性线索和外周线索都具有反射性注意定向这一特点,社会性注意往往也被认为属于外源性注意.但是,外源性注意并不能完全解释所有的社会性注意现象.因此,两者是否具有相同的加工机制,尚存在争论.方法 本研究使用空间线索范式,系统考察了线索有效...     

Coordinates of Human Visual and Inertial Heading Perception

Heading estimation involves both inertial and visual cues. Inertial motion is sensed by the labyrinth, somatic sensation by the body, and optic flow by the retina. Because the eye and head are mobile these stimuli are sensed relative to different reference frames and it remains unclear if a perception occurs in a common reference frame. Recent neurophysiologic evidence has suggested the reference frames remain separate even at higher levels of processing but has not addressed the resulting perception. Seven human subjects experienced a 2s, 16 cm/s translation and/or a visual stimulus corresponding with this translation. For each condition 72 stimuli (360° in 5° increments) were delivered in random order. After each stimulus the subject identified the perceived heading using a mechanical dial. Some trial blocks included interleaved conditions in which the influence of ±28° of gaze and/or head position were examined. The observations were fit using a two degree-of-freedom population vector decoder (PVD) model which considered the relative sensitivity to lateral motion and coordinate system offset. For visual stimuli gaze shifts caused shifts in perceived head estimates in the direction opposite the gaze shift in all subjects. These perceptual shifts averaged 13 ± 2° for eye only gaze shifts and 17 ± 2° for eye-head gaze shifts. This finding indicates visual headings are biased towards retina coordinates. Similar gaze and head direction shifts prior to inertial headings had no significant influence on heading direction. Thus inertial headings are perceived in body-centered coordinates. Combined visual and inertial stimuli yielded intermediate results.     

Gaze following in human infants depends on communicative signals

Humans are extremely sensitive to ostensive signals, like eye contact or having their name called, that indicate someone's communicative intention toward them [1-3]. Infants also pay attention to these signals [4-6], but it is unknown whether they appreciate their significance in the initiation of communicative acts. In two experiments, we employed video presentation of an actor turning toward one of two objects and recorded infants' gaze-following behavior [7-13] with eye-tracking techniques [11, 12]. We found that 6-month-old infants followed the adult's gaze (a potential communicative-referential signal) toward an object only when such an act is preceded by ostensive cues such as direct gaze (experiment 1) and infant-directed speech (experiment 2). Such a link between the presence of ostensive signals and gaze following suggests that this behavior serves a functional role in assisting infants to effectively respond to referential communication directed to them. Whereas gaze following in many nonhuman species supports social information gathering [14-18], in humans it initially appears to reflect the expectation of a more active, communicative role from the information source.     

Visual co-orientation and expectations about attentional orientation in pileated gibbons (Hylobates pileatus)

This study investigated attentional processes in a sample of captive gibbons. An initial aim of the research was to examine subjects' ability to co-orient with photographic images of both conspecific and human models. The gibbons' expectancies about the focus of another's attention was then also assessed, with an expectancy violation paradigm revealing subjects' sensitivity to an incompatibility between visual orientation and the position of a target object. The gibbons were exposed to two conditions; consistent sequences in which the stimulus individual directed attention towards a target object, and inconsistent sequences in which the model's attentional focus was incompatible with the location of this article. Analyses of the subjects' responses were made according to the direction of gazes and the time spent inspecting the depicted model in each of these conditions. The results reveal a tendency for visual co-orientation with both conspecific and human models, suggesting that gibbons are competent in detecting the visual orientation of other species as well as their own. Furthermore, the subjects' tendency to look longer and check back to the depicted model in response to violations in the relationship between an agent and object (target appearing in an opposite direction to model's gaze), suggests that they possess some knowledge of how visual gaze direction relates to external stimuli.     

Postural Sway and Gaze Can Track the Complex Motion of a Visual Target

Variability is an inherent and important feature of human movement. This variability has form exhibiting a chaotic structure. Visual feedback training using regular predictive visual target motions does not take into account this essential characteristic of the human movement, and may result in task specific learning and loss of visuo-motor adaptability. In this study, we asked how well healthy young adults can track visual target cues of varying degree of complexity during whole-body swaying in the Anterior-Posterior (AP) and Medio-Lateral (ML) direction. Participants were asked to track three visual target motions: a complex (Lorenz attractor), a noise (brown) and a periodic (sine) moving target while receiving online visual feedback about their performance. Postural sway, gaze and target motion were synchronously recorded and the degree of force-target and gaze-target coupling was quantified using spectral coherence and Cross-Approximate entropy. Analysis revealed that both force-target and gaze-target coupling was sensitive to the complexity of the visual stimuli motions. Postural sway showed a higher degree of coherence with the Lorenz attractor than the brown noise or sinusoidal stimulus motion. Similarly, gaze was more synchronous with the Lorenz attractor than the brown noise and sinusoidal stimulus motion. These results were similar regardless of whether tracking was performed in the AP or ML direction. Based on the theoretical model of optimal movement variability tracking of a complex signal may provide a better stimulus to improve visuo-motor adaptation and learning in postural control.     

Predicting Aggressive Tendencies by Visual Attention Bias Associated with Hostile Emotions

The goal of the current study is to clarify the relationship between social information processing (e.g., visual attention to cues of hostility, hostility attribution bias, and facial expression emotion labeling) and aggressive tendencies. Thirty adults were recruited in the eye-tracking study that measured various components in social information processing. Baseline aggressive tendencies were measured using the Buss-Perry Aggression Questionnaire (AQ). Visual attention towards hostile objects was measured as the proportion of eye gaze fixation duration on cues of hostility. Hostility attribution bias was measured with the rating results for emotions of characters in the images. The results show that the eye gaze duration on hostile characters was significantly inversely correlated with the AQ score and less eye contact with an angry face. The eye gaze duration on hostile object was not significantly associated with hostility attribution bias, although hostility attribution bias was significantly positively associated with the AQ score. Our findings suggest that eye gaze fixation time towards non-hostile cues may predict aggressive tendencies.     

Measurement of eye-gaze in chimpanzees (Pan troglodytes)

Gaze cues are used as an index of social cognition in primates, yet the sensitivity to different forms of gaze, and consequently the cues required to test gaze-following abilities remain understudied. Whereas the eye is attributed special signal value in humans, the camouflaged ocular morphology of non-human primates has led to the consensus that head orientation may be a more salient cue. This study presents the first documentation of the surface eye movements of the chimpanzee, Pan troglodytes, in order to determine the behavioral forms of eye-gaze and their saliency as signals, document their functional variation, and address the signal value of the eyes distinct from head orientation. Movements of the eye were identified as Scan (continuous movement), Glance (a single movement <1 sec), or Fixate (no movement). Scans, glances, and fixations were reliably detected by humans during live observation and from video (Cohen's kappa over 0.70) and, therefore, are likely also to be detected by conspecifics. Eye-gaze comprised a nonunitary measure of visual attention, reflecting the attentional task demands of different activities. Specifically, chimpanzees spent significantly more time scanning while feeding and resting, than grooming, F(2,28) = 10.23, P<0.001, and spent significantly more time fixating while grooming, than feeding or resting, F(2,28) = 7.52, P<0.01. Further, eye-gaze was often incongruent with head movement, varying significantly with the form of eye-gaze: incongruence was found during 12-21% of fixations, during 42-49% of scans, and during 70-100% of glances, F(2,16) = 30.17, P<0.001. These findings provide the basis for discrimination of the adaptive significance of gaze-processing abilities with emphasis on sensitivity to eye-gaze distinct from head orientation. If we are to continue exploring gaze-processing abilities in primates, then we need greater consideration of the precise nature of the signals themselves. Here we present evidence for special consideration of the eyes as a salient signal in P. troglodytes.     

Decoupled Visually-Guided Reaching in Optic Ataxia: Differences in Motor Control between Canonical and Non-Canonical Orientations in Space

Guiding a limb often involves situations in which the spatial location of the target for gaze and limb movement are not congruent (i.e. have been decoupled). Such decoupled situations involve both the implementation of a cognitive rule (i.e. strategic control) and the online monitoring of the limb position relative to gaze and target (i.e. sensorimotor recalibration). To further understand the neural mechanisms underlying these different types of visuomotor control, we tested patient IG who has bilateral caudal superior parietal lobule (SPL) damage resulting in optic ataxia (OA), and compared her performance with six age-matched controls on a series of center-out reaching tasks. The tasks comprised 1) directing a cursor that had been rotated (180° or 90°) within the same spatial plane as the visual display, or 2) moving the hand along a different spatial plane than the visual display (horizontal or para-sagittal). Importantly, all conditions were performed towards visual targets located along either the horizontal axis (left and right; which can be guided from strategic control) or the diagonal axes (top-left and top-right; which require on-line trajectory elaboration and updating by sensorimotor recalibration). The bilateral OA patient performed much better in decoupled visuomotor control towards the horizontal targets, a canonical situation in which well-categorized allocentric cues could be utilized (i.e. guiding cursor direction perpendicular to computer monitor border). Relative to neurologically intact adults, IG''s performance suffered towards diagonal targets, a non-canonical situation in which only less-categorized allocentric cues were available (i.e. guiding cursor direction at an off-axis angle to computer monitor border), and she was therefore required to rely on sensorimotor recalibration of her decoupled limb. We propose that an intact caudal SPL is crucial for any decoupled visuomotor control, particularly when relying on the realignment between vision and proprioception without reliable allocentric cues towards non-canonical orientations in space.     

Reflexive social attention in monkeys and humans

For humans, social cues often guide the focus of attention. Although many nonhuman primates, like humans, live in large, complex social groups, the extent to which human and nonhuman primates share fundamental mechanisms of social attention remains unexplored. Here, we show that, when viewing a rhesus macaque looking in a particular direction, both rhesus macaques and humans reflexively and covertly orient their attention in the same direction. Specifically, when performing a peripheral visual target detection task, viewing a monkey with either its eyes alone or with both its head and eyes averted to one side facilitated the detection of peripheral targets when they randomly appeared on the same side. Moreover, viewing images of a monkey with averted gaze evoked small but systematic shifts in eye position in the direction of gaze in the image. The similar magnitude and temporal dynamics of response facilitation and eye deviation in monkeys and humans suggest shared neural circuitry mediating social attention.     

Intergroup threat gates social attention in humans

Humans shift their attention to follow another person''s gaze direction, a phenomenon called gaze cueing. This study examined whether a particular social factor, intergroup threat, modulates gaze cueing. As expected, stronger responses of a particular in-group to a threatening out-group were observed when the in-group, conditioned to perceive threat from one of two out-groups, was presented with facial stimuli from the threatening and non-threatening out-groups. These results suggest that intergroup threat plays an important role in shaping social attention. Furthermore, larger gaze-cueing effects were found for threatening out-group faces than for in-group faces only at the 200 ms but not the 800 ms stimulus onset asynchrony (SOA); the specificity of the gaze-cueing effects at the short SOA suggests that threat cues modulate the involuntary component of gaze cueing.     

Functional specialization of mouse higher visual cortical areas

The mouse is emerging as an important model for understanding how sensory neocortex extracts cues to guide behavior, yet little is known about how these cues are processed beyond primary cortical areas. Here, we used two-photon calcium imaging in awake mice to compare visual responses in primary visual cortex (V1) and in two downstream target areas, AL and PM. Neighboring V1 neurons had diverse stimulus preferences spanning five octaves in spatial and temporal frequency. By contrast, AL and PM neurons responded best to distinct ranges of stimulus parameters. Most strikingly, AL neurons preferred fast-moving stimuli while PM neurons preferred slow-moving stimuli. By contrast, neurons in V1, AL, and PM demonstrated similar selectivity for stimulus orientation but not for stimulus direction. Based on these findings, we predict that area AL helps guide behaviors involving fast-moving stimuli (e.g., optic flow), while area PM?helps guide behaviors involving slow-moving objects.     

Subtle cues of predation risk: starlings respond to a predator's direction of eye-gaze

For prey animals to negotiate successfully the fundamental trade-off between predation and starvation, a realistic assessment of predation risk is vital. Prey responses to conspicuous indicators of risk (such as looming predators or fleeing conspecifics) are well documented, but there should also be strong selection for the detection of more subtle cues. A predator's head orientation and eye-gaze direction are good candidates for subtle but useful indicators of risk, since many predators orient their head and eyes towards their prey as they attack. We describe the first explicit demonstration of a bird responding to a live predator's eye-gaze direction. We present wild-caught European starlings (Sturnus vulgaris) with human 'predators' whose frontal appearance and gaze direction are manipulated independently, and show that starlings are sensitive to the predator's orientation, the presence of eyes and the direction of eye-gaze. Starlings respond in a functionally significant manner: when the predator's gaze was averted, starlings resumed feeding earlier, at a higher rate and consumed more food overall. By correctly assessing lower risk and returning to feeding activity earlier (as in this study), the animal gains a competitive advantage over conspecifics that do not respond to the subtle predator cue in this way.     

Influence of a Capuchin Monkey Companion on the Social Life of a Person with Quadriplegia: An Experimental Study

ABSTRACT

As a consequence of a severe reduction in their autonomy, the social life of people with quadriplegia becomes highly routine. In addition, the social environment becomes very limited because people without disabilities may feel awkward around, or have an aversion to, people with quadriplegia. A pet animal often facilitates social interactions between humans, and in this study we investigated the influence of a capuchin monkey companion on the social environment of a person with quadriplegia. In three different public areas, we compared the behaviors of passers-by confronted with a person with quadriplegia or a person who had no disabilities, either alone or with a capuchin companion. In both situations the capuchin companion greatly modified the behaviors of the passers-by, inducing more positive social behaviors such as smiles, and higher frequencies of visual contact. In addition, passers-by tended to avoid the person with quadriplegia less often when the capuchin was present. The presence of a capuchin companion potentially improves the social environment of people with quadriplegia.     

Eye-Head Coordination for Visual Cognitive Processing

We investigated coordinated movements between the eyes and head (“eye-head coordination”) in relation to vision for action. Several studies have measured eye and head movements during a single gaze shift, focusing on the mechanisms of motor control during eye-head coordination. However, in everyday life, gaze shifts occur sequentially and are accompanied by movements of the head and body. Under such conditions, visual cognitive processing influences eye movements and might also influence eye-head coordination because sequential gaze shifts include cycles of visual processing (fixation) and data acquisition (gaze shifts). In the present study, we examined how the eyes and head move in coordination during visual search in a large visual field. Subjects moved their eyes, head, and body without restriction inside a 360° visual display system. We found patterns of eye-head coordination that differed those observed in single gaze-shift studies. First, we frequently observed multiple saccades during one continuous head movement, and the contribution of head movement to gaze shifts increased as the number of saccades increased. This relationship between head movements and sequential gaze shifts suggests eye-head coordination over several saccade-fixation sequences; this could be related to cognitive processing because saccade-fixation cycles are the result of visual cognitive processing. Second, distribution bias of eye position during gaze fixation was highly correlated with head orientation. The distribution peak of eye position was biased in the same direction as head orientation. This influence of head orientation suggests that eye-head coordination is involved in gaze fixation, when the visual system processes retinal information. This further supports the role of eye-head coordination in visual cognitive processing.     

Northern bald ibises follow others’ gaze into distant space but not behind barriers

Gaze following is the ability to use the visual orientation of others as a trigger to look in the same direction. Thereby, animals may either align their head and eye orientation with others (gaze following into distant space) or may even reposition themselves to look behind barriers impairing their perception (geometrical gaze following). It has been proposed that these two different modes are functionally and cognitively distinct, but experimental evidence for this claim is lacking. We here, to our knowledge, demonstrate for the first time, that adult animals may be capable of following gaze into distant space, but not geometrically around barriers. We tested Northern bald ibises (Geronticus eremita) for their ability to follow a conspecific''s gaze in two standard tasks. The birds readily looked up after seeing a model bird looking up; however, when seeing a model looking behind a barrier, they responded by looking at the barrier instead of walking around. These findings are in stark contrast to results obtained with great apes and corvids and provide the first experimental evidence, to our knowledge, for cognitive differences in gaze following tasks.