Species difference in the timing of gaze movement between chimpanzees and humans

How do humans and their closest relatives, chimpanzees, differ in their fundamental abilities for seeing the visual world? In this study, we directly compared the gaze movements of humans and the closest species, chimpanzees, using an eye-tracking system. During free viewing of a naturalistic scene, chimpanzees made more fixations per second (up to four) than did humans (up to three). This species difference was independent of the semantic variability of the presented scenes. The gap–overlap paradigm revealed that, rather than resulting from the sensitivity to the peripherally presented stimuli per se, the species difference reflected the particular strategy each species employed to solve the rivalry between central (fixated) and peripheral stimuli in their visual fields. Finally, when presented with a movie in which small images successively appeared/disappeared at random positions at the chosen presentation rate, chimpanzees tracked those images at the point of fixation for a longer time than did humans, outperforming humans in their speed of scanning. Our results suggest that chimpanzees and humans differ quantitatively in their visual strategies involving the timing of gaze movement. We discuss the functional reasons for each species’ employing such specific strategies.     

自闭症谱系障碍儿童在多重线索下习得词语的眼动研究

本文利用眼动追踪技术在基线、一致和矛盾3种实验条件下考察感知觉线索和社会性线索在自闭症谱系障碍儿童词语习得中的相对作用。行为数据结果表明, 此类儿童在矛盾条件下选择枯燥物体作为新异词语的所指对象, 这说明社会性线索较之于感知觉线索具有优势作用; 而他们在基线和一致条件下选择有趣物体作为新异词语的所指对象, 且一致条件的词语习得成绩优于基线条件, 这说明社会性线索较之于感知觉线索具有促进作用。眼动数据结果表明, 此类儿童在脸部注视模式和视线追随行为上与普通儿童存在差异。这说明, 虽然社会性线索在此类儿童与普通儿童的词语习得中具有相同的相对作用, 但他们获取社会性信息的方式与普通儿童存在差异。     

Stream/bounce perception and the effect of depth cues in chimpanzees (Pan troglodytes)

The stream/bounce display represents an ambiguous motion event in which two identical visual objects move toward one another and the objects overlap completely before they pass each another. In our perception, they can be interpreted as either streaming past one another or bouncing off each other. Previous studies have shown that the streaming percept of the display is generic for humans, suggesting the inertial nature of the motion integration process. In this study, chimpanzees took part in behavioral experiments using an object-tracking task to reveal the characteristics of their stream/bounce perception. Chimpanzees did not show a tendency toward a dominant "stream" perception of the stream/bounce stimulus. However, depth cues, such as X-junctions and local motion coherence, did promote the stream percept in chimpanzees. These results suggest both similarities and differences between chimpanzees and humans with respect to motion integration and object individuation processes.     

Gaze motion clustering in scan-path estimation

Visual attention is considered nowadays a paramount ability both in Cognitive Sciences and in Cognitive Vision to bridge the gap between perception and higher level reasoning functions, such as scene interpretation and decision making. Bottom-up gaze shifting is the main mechanism used by humans when exploring a scene without a specific task. In this paper we investigated which criteria allow for the generation of plausible fixation clusters by analysing experimental data of human subjects. We suggest that fixations should be grouped in cliques whose saliency can be assessed through an innovation factor encompassing bottom-up cues, proximity, direction and memory components.     

Enhanced perceptual processing of speech in autism

Theories of autism have proposed that a bias towards low-level perceptual information, or a featural/surface-biased information-processing style, may compromise higher-level language processing in such individuals. Two experiments, utilizing linguistic stimuli with competing low-level/perceptual and high-level/semantic information, tested processing biases in children with autism and matched controls. Whereas children with autism exhibited superior perceptual processing of speech relative to controls, and showed no evidence of either a perceptual or semantic processing bias, controls showed a tendency to process speech semantically. The data provide partial support to the perceptual theories of autism. It is additionally proposed that the pattern of results may reflect different patterns of attentional focusing towards single or multiple stimulus cues in speech between children with autism and controls.     

The perception of unfamiliar faces and houses by chimpanzees: influence of rotation angle

The inversion effect, or impaired recognition of upside-down faces, is used as evidence supporting the configural processing of faces. Human studies report a linear relationship between face-discrimination performance and orientation, such that recognition is more difficult as faces are rotated away from their typical viewpoint. Previous studies on chimpanzees also support a configural bias for processing faces, particularly faces for which subjects have developed expertise. In the present study, we examined the influence of expertise and rotation angle on the visual perception of faces in chimpanzees. Six subjects were presented with unaltered and blurred conspecific faces and houses in five orientation angles. A computerized paradigm was used to further delineate the nature of configural face processing in this species. The data were consistent with those reported in humans: chimpanzees showed a significant linear impairment when discriminating conspecific faces as they rotated away from their upright orientation. No inversion effect was observed for discriminations involving houses. Thus, chimpanzees, like humans, show a face-specific inversion effect that is linearly affected by angle of orientation, suggesting that their visual processing of faces is strongly influenced by the extraction of configural cues and closely resembles the perceptual strategies of humans.     

Is chimpanzee (Pan troglodytes) spatial attention reflexively triggered by gaze cue?

Humans show a reflexive shift in spatial attention triggered by gaze cues. Chimpanzees (Pan troglodytes) have an excellent ability to follow another's gaze, but they exhibit a limited capacity to engage in triadic interactions based on joint attention, suggesting the possibility of contributions of the different mechanisms underlying joint attention between humans and chimpanzees. The present study thus examined how the chimpanzee's visual spatial attention is triggered by gaze cues. Two chimpanzees showed no clear signs of attention shift triggered by various kinds of nonfacial and facial stimuli with averted gaze under the letter-discrimination tasks but showed significant cueing effects when the head-turning cue was presented in a quasi-dynamic manner. These cueing effects were, however, affected by the predictability of the gaze cue: Highly predictive gaze cues caused stronger cueing effects than less predictive cues. Thus, these results suggest that the shift in spatial attention caused by gaze cues does occur in chimpanzees, but, in contrast to humans, vulnerability against the cue predictability suggests that the voluntary mechanism contributes more dominantly than the reflexive mechanism to this attention shift.     

The organization of conspecific face space in nonhuman primates

Humans and chimpanzees demonstrate numerous cognitive specializations for processing faces, but comparative studies with monkeys suggest that these may be the result of recent evolutionary adaptations. The present study utilized the novel approach of face space, a powerful theoretical framework used to understand the representation of face identity in humans, to further explore species differences in face processing. According to the theory, faces are represented by vectors in a multidimensional space, the centre of which is defined by an average face. Each dimension codes features important for describing a face's identity, and vector length codes the feature's distinctiveness. Chimpanzees and rhesus monkeys discriminated male and female conspecifics’ faces, rated by humans for their distinctiveness, using a computerized task. Multidimensional scaling analyses showed that the organization of face space was similar between humans and chimpanzees. Distinctive faces had the longest vectors and were the easiest for chimpanzees to discriminate. In contrast, distinctiveness did not correlate with the performance of rhesus monkeys. The feature dimensions for each species’ face space were visualized and described using morphing techniques. These results confirm species differences in the perceptual representation of conspecific faces, which are discussed within an evolutionary framework.     

Trial-by-trial adjustments in control triggered by incidentally encoded semantic cues

Cognitive control mechanisms provide the flexibility to rapidly adapt to contextual demands. These contexts can be defined by top-down goals—but also by bottom-up perceptual factors, such as the location at which a visual stimulus appears. There are now several experiments reporting contextual control effects. Such experiments establish that contexts defined by low-level perceptual cues such as the location of a visual stimulus can lead to context-specific control, suggesting a relatively early focus for cognitive control. The current set of experiments involved a word–word interference task designed to assess whether a high-level cue, the semantic category to which a word belongs, can also facilitate contextual control. Indeed, participants exhibit a larger Flanker effect to items pertaining to a semantic category in which 75% of stimuli are incongruent than in response to items pertaining to a category in which 25% of stimuli are incongruent. Thus, both low-level and high-level stimulus features can affect the bottom-up engagement of cognitive control. The implications for current models of cognitive control are discussed.     

Carryover effect of joint attention to repeated events in chimpanzees and young children

Gaze following is a fundamental component of triadic social interaction which includes events and an object shared with other individuals and is found in both human and nonhuman primates. Most previous work has focused only on the immediate reaction after following another’s gaze. In contrast, this study investigated whether gaze following is retained after the observation of the other’s gaze shift, whether this retainment differs between species and age groups, and whether the retainment depends on the nature of the preceding events. In the social condition, subjects (1- and 2-year-old human children and chimpanzees) witnessed an experimenter who looked and pointed in the direction of a target lamp. In the physical condition, the target lamp blinked but the experimenter did not provide any cues. After a brief delay, we presented the same stimulus again without any cues. All subjects looked again to the target location after experiencing the social condition and thus showed a carryover effect. However, only 2-year-olds showed a carryover effect in the physical condition; 1-year-olds and chimpanzees did not. Additionally, only human children showed spontaneous interactive actions such as pointing. Our results suggest that the difference between the two age groups and chimpanzees is conceptual and not only quantitative.     

Memory for scenes: Refixations reflect retrieval

Most conceptions of episodic memory hold that reinstatement of encoding operations is essential for retrieval success, but the specific mechanisms of retrieval reinstatement are not well understood. In three experiments, we used saccadic eye movements as a window for examining reinstatement in scene recognition. In Experiment 1, participants viewed complex scenes, while number of study fixations was controlled by using a gaze-contingent paradigm. In Experiment 2, effects of stimulus saliency were minimized by directing participants' eye movements during study. At test, participants made remember/know judgments for each recognized stimulus scene. Both experiments showed that remember responses were associated with more consistent study-test fixations than false rejections (Experiments 1 and 2) and know responses (Experiment 2). In Experiment 3, we examined the causal role of gaze consistency on retrieval by manipulating participants' expectations during recognition. After studying name and scene pairs, each test scene was preceded by the same or different name as during study. Participants made more consistent eye movements following a matching, rather than mismatching, scene name. Taken together, these findings suggest that explicit recollection is a function of perceptual reconstruction and that event memory influences gaze control in this active reconstruction process.     

Perception of complex geometric figures in chimpanzees (Pan troglodytes) and humans (Homo sapiens): analyses of visual similarity on the basis of choice reaction time.

In a conditional-discrimination task (matching-to-sample), we assessed similarities among figures consisting of 2 elemental figures through the choice reaction time, nonmetric multidimensional scaling, and hierarchical cluster analysis data from chimpanzees (Pan troglodytes) and humans (Homo sapiens). Humans also rated similarities among figures. The results of the 3 experiments clearly indicated that the reaction time data obtained from chimpanzees' performances were useful measures of the similarities among figures. The results suggested that chimpanzees and humans perceived the complex figures similarly. The outer-contour elements were perceived most dominantly by both species, and the straight-line elements were perceived least dominantly. Both species showed the same perceptual hierarchy or dominance among perceptual categories, as determined by the similarity of simple elements, on the basis of transformational invariances.     

Consistent left gaze bias in processing different facial cues

While viewing faces, humans often demonstrate a natural gaze bias towards the left visual field, that is, the right side of the viewee’s face is often inspected first and for longer periods. Previous studies have suggested that this gaze asymmetry is a part of the gaze pattern associated with face exploration, but its relation with perceptual processing of facial cues is unclear. In this study we recorded participants’ saccadic eye movements while exploring face images under different task instructions (free viewing, judging familiarity and judging facial expression). We observed a consistent left gaze bias in face viewing irrespective of task demands. The probability of the first fixation and the proportion of overall fixations directed at the left hemiface were indistinguishable across different task instructions or across different facial expressions. It seems that the left gaze bias is an automatic reflection of hemispheric lateralisation in face processing, and is not necessarily correlated with the perceptual processing of a specific type of facial information.     

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

The previous studies have shown that human infants and domestic dogs follow the gaze of a human agent only when the agent has addressed them ostensively—e.g., by making eye contact, or calling their name. This evidence is interpreted as showing that they expect ostensive signals to precede referential information. The present study tested chimpanzees, one of the closest relatives to humans, in a series of eye-tracking experiments using an experimental design adapted from these previous studies. In the ostension conditions, a human actor made eye contact, called the participant’s name, and then looked at one of two objects. In the control conditions, a salient cue, which differed in each experiment (a colorful object, the actor’s nodding, or an eating action), attracted participants’ attention to the actor’s face, and then the actor looked at the object. Overall, chimpanzees followed the actor’s gaze to the cued object in both ostension and control conditions, and the ostensive signals did not enhance gaze following more than the control attention-getters. However, the ostensive signals enhanced subsequent attention to both target and distractor objects (but not to the actor’s face) more strongly than the control attention-getters—especially in the chimpanzees who had a close relationship with human caregivers. We interpret this as showing that chimpanzees have a simple form of communicative expectations on the basis of ostensive signals, but unlike human infants and dogs, they do not subsequently use the experimenter’s gaze to infer the intended referent. These results may reflect a limitation of non-domesticated species for interpreting humans’ ostensive signals in inter-species communication.     

Chimpanzee Use of Human and Conspecific Social Cues to Locate Hidden Food

Two studies are reported in which chimpanzees attempted to use social cues to locate hidden food in one of two possible hiding places. In the first study four chimpanzees were exposed to a local enhancement cue (the informant approached and looked to the location where food was hidden and then remained beside it) and a gaze/point cue (the informant gazed and manually pointed towards the location where the food was hidden). Each cue was given by both a human informant and a chimpanzee informant. In the second study 12 chimpanzees were exposed to a gaze direction cue in combination with a vocal cue (the human informant gazed to the hiding location and produced one of two different vocalizations: a ‘food-bark’ or a human word-form). The results were: (i) all subjects were quite skillful with the local enhancement cue, no matter who produced it; (ii) few subjects were skillful with the gaze/point cue, no matter who produced it (most of these being individuals who had been raised in infancy by humans); and (iii) most subjects were skillful when the human gazed and vocalized at the hiding place, with little difference between the two types of vocal cue. Findings are discussed in terms of chimpanzees’ apparent need for additional cues, over and above gaze direction cues, to indicate the presence of food.     

Influence of semantic consistency and perceptual features on visual attention during scene viewing in toddlers

Conceptual representations of everyday scenes are built in interaction with visual environment and these representations guide our visual attention. Perceptual features and object-scene semantic consistency have been found to attract our attention during scene exploration. The present study examined how visual attention in 24-month-old toddlers is attracted by semantic violations and how perceptual features (i. e. saliency, centre distance, clutter and object size) and linguistic properties (i. e. object label frequency and label length) affect gaze distribution. We compared eye movements of 24-month-old toddlers and adults while exploring everyday scenes which either contained an inconsistent (e.g., soap on a breakfast table) or consistent (e.g., soap in a bathroom) object. Perceptual features such as saliency, centre distance and clutter of the scene affected looking times in the toddler group during the whole viewing time whereas looking times in adults were affected only by centre distance during the early viewing time. Adults looked longer to inconsistent than consistent objects either if the objects had a high or a low saliency. In contrast, toddlers presented semantic consistency effect only when objects were highly salient. Additionally, toddlers with lower vocabulary skills looked longer to inconsistent objects while toddlers with higher vocabulary skills look equally long to both consistent and inconsistent objects. Our results indicate that 24-month-old children use scene context to guide visual attention when exploring the visual environment. However, perceptual features have a stronger influence in eye movement guidance in toddlers than in adults. Our results also indicate that language skills influence cognitive but not perceptual guidance of eye movements during scene perception in toddlers.     

Preference for human direct gaze in infant chimpanzees (Pan troglodytes)

We studied gaze perception in three infant chimpanzees (Pan troglodytes), aged 10-32 weeks, using a two-choice preferential-looking paradigm. The infants were presented with two photographs of a human face: (a) with the eyes open or closed, and (b) with a direct or an averted gaze. We found that the chimpanzees preferred looking at the direct-gaze face. However, in the context of scrambled faces, the infants showed no difference in gaze discrimination between direct and averted gazes. These findings suggest that gaze perception by chimpanzees may be influenced by the surrounding facial context. The relationship between gaze perception, face processing, and the adaptive significance of gaze perception are discussed from an evolutionary perspective.     

Mid-level feature contributions to category-specific gaze guidance

Our research has previously shown that scene categories can be predicted from observers’ eye movements when they view photographs of real-world scenes. The time course of category predictions reveals the differential influences of bottom-up and top-down information. Here we used these known differences to determine to what extent image features at different representational levels contribute toward guiding gaze in a category-specific manner. Participants viewed grayscale photographs and line drawings of real-world scenes while their gaze was tracked. Scene categories could be predicted from fixation density at all times over a 2-s time course in both photographs and line drawings. We replicated the shape of the prediction curve found previously, with an initial steep decrease in prediction accuracy from 300 to 500 ms, representing the contribution of bottom-up information, followed by a steady increase, representing top-down knowledge of category-specific information. We then computed the low-level features (luminance contrasts and orientation statistics), mid-level features (local symmetry and contour junctions), and Deep Gaze II output from the images, and used that information as a reference in our category predictions in order to assess their respective contributions to category-specific guidance of gaze. We observed that, as expected, low-level salience contributes mostly to the initial bottom-up peak of gaze guidance. Conversely, the mid-level features that describe scene structure (i.e., local symmetry and junctions) split their contributions between bottom-up and top-down attentional guidance, with symmetry contributing to both bottom-up and top-down guidance, while junctions play a more prominent role in the top-down guidance of gaze.     

Quantifying the contribution of low-level saliency to human eye movements in dynamic scenes

We investigated the contribution of low-level saliency to human eye movements in complex dynamic scenes. Eye movements were recorded while naive observers viewed a heterogeneous collection of 50 video clips (46,489 frames; 4-6 subjects per clip), yielding 11,916 saccades of amplitude ≥2°. A model of bottom-up visual attention computed instantaneous saliency at the instant each saccade started and at its future endpoint location. Median model-predicted saliency was 45% the maximum saliency, a significant factor 2.03 greater than expected by chance. Motion and temporal change were stronger predictors of human saccades than colour, intensity, or orientation features, with the best predictor being the sum of all features. There was no significant correlation between model-predicted saliency and duration of fixation. A majority of saccades were directed to a minority of locations reliably marked as salient by the model, suggesting that bottom-up saliency may provide a set of candidate saccade target locations, with the final choice of which location of fixate more strongly determined top-down.     

Discrimination of contour-deleted images in baboons (<Emphasis Type="Italic">Papio papio</Emphasis>) and chimpanzees (<Emphasis Type="Italic">Pan troglodytes</Emphasis>)

Humans readily group component elements into a coherent perceptual whole and perceive the global form of visual patterns in priority over local features, which stands in contrast to at least some data from the animal literature, suggesting possible species differences in perceptual processes. In this study, chimpanzees and baboons were required to match intact and partially contour-deleted line-drawings in a computerized task in order to further explore the ability of nonhuman primates to group component elements into a coherent perceptual whole and to determine to what extent they use the global form or the local features. Experiment 1 showed that the baboons and chimpanzees matched intact continuous line-drawings (intact-intact) more easily than partially contour-deleted line-drawings (deleted-deleted). Both species could also match partially deleted line-drawings with their intact version (deleted-intact), but at a lower performance level. Experiment 2 further showed that subjects from the two species could match partially deleted coherent line-drawings (deleted-deleted) more easily than their scrambled incoherent versions (scrambled-scrambled). They could however match the coherent deleted forms with their scrambled version (deleted-scrambled). It is suggested that solutions of these tasks rely on the processing of both global and local cues, with no clear-cut species difference in that ability. Overall, the results show that contour completion of line-drawings was not easy. Implications on the processing of human-made two-dimensional representations such as line-drawings are discussed.