Visual Search for Human Gaze Direction by a Chimpanzee (Pan troglodytes)

Background

Humans detect faces with direct gazes among those with averted gazes more efficiently than they detect faces with averted gazes among those with direct gazes. We examined whether this “stare-in-the-crowd” effect occurs in chimpanzees (Pan troglodytes), whose eye morphology differs from that of humans (i.e., low-contrast eyes, dark sclera).

Methodology/Principal Findings

An adult female chimpanzee was trained to search for an odd-item target (front view of a human face) among distractors that differed from the target only with respect to the direction of the eye gaze. During visual-search testing, she performed more efficiently when the target was a direct-gaze face than when it was an averted-gaze face. This direct-gaze superiority was maintained when the faces were inverted and when parts of the face were scrambled. Subsequent tests revealed that gaze perception in the chimpanzee was controlled by the contrast between iris and sclera, as in humans, but that the chimpanzee attended only to the position of the iris in the eye, irrespective of head direction.

Conclusion/Significance

These results suggest that the chimpanzee can discriminate among human gaze directions and are more sensitive to direct gazes. However, limitations in the perception of human gaze by the chimpanzee are suggested by her inability to completely transfer her performance to faces showing a three-quarter view.     

Searching for asymmetries in the detection of gaze contact versus averted gaze under different head views: a behavioural study

Eye contact is a crucial social cue constituting a frequent preliminary to interaction. Thus, the perception of others' gaze may be associated with specific processes beginning with asymmetries in the detection of direct versus averted gaze. We tested this hypothesis in two behavioural experiments using realistic eye stimuli in a visual search task. We manipulated the head orientation (frontal or deviated) and the visual field (right or left) in which the target appeared at display onset. We found that direct gaze targets presented among averted gaze distractors were detected faster and better than averted gaze targets among direct gaze distractors, but only when the head was deviated. Moreover, direct gaze targets were detected very quickly and efficiently regardless of head orientation and visual field, whereas the detection of averted gaze was strongly modulated by these factors. These results suggest that gaze contact has precedence over contextual information such as head orientation and visual field.     

Is object search mediated by object-based or image-based representations?

Recent research suggests that visually specific memory representations for previously fixated objects are maintained during scene perception. Here we investigate the degree of visual specificity by asking whether the memory representations are image-based or object-based. To that end we measured the effects of object orientation on the time to search for a familiar object from amongst a set of 7 familiar distractors arranged in a circular array. Search times were found to depend on the relative orientations of the target object and the probe object for both familiar and novel objects. This effect was found to be partly an image matching effect but there was also an advantage shown for the object's canonical view for familiar objects. Orientation effects were maintained even when the target object was specified as having unique or similar shape properties relative to the distractors. Participants' eye movements were monitored during two of the experiments. Eye movement patterns revealed selection for object shape and object orientation during the search process. Our findings provide evidence for object representations during search that are detailed and share image-based characteristics with more high-level characteristics from object memory.     

Determinants of Dwell Time in Visual Search: Similarity or Perceptual Difficulty?

The present study examined the factors that determine the dwell times in a visual search task, that is, the duration the gaze remains fixated on an object. It has been suggested that an item's similarity to the search target should be an important determiner of dwell times, because dwell times are taken to reflect the time needed to reject the item as a distractor, and such discriminations are supposed to be harder the more similar an item is to the search target. In line with this similarity view, a previous study shows that, in search for a target ring of thin line-width, dwell times on thin linewidth Landolt C's distractors were longer than dwell times on Landolt C's with thick or medium linewidth. However, dwell times may have been longer on thin Landolt C's because the thin line-width made it harder to detect whether the stimuli had a gap or not. Thus, it is an open question whether dwell times on thin line-width distractors were longer because they were similar to the target or because the perceptual decision was more difficult. The present study de-coupled similarity from perceptual difficulty, by measuring dwell times on thin, medium and thick line-width distractors when the target had thin, medium or thick line-width. The results showed that dwell times were longer on target-similar than target-dissimilar stimuli across all target conditions and regardless of the line-width. It is concluded that prior findings of longer dwell times on thin linewidth-distractors can clearly be attributed to target similarity. As will be discussed towards the end, the finding of similarity effects on dwell times has important implications for current theories of visual search and eye movement control.     

From unicellularity to multicellularity - molecular speculations about early animal evolution

A morphological, physiological, developmental, and genetic organization of great complexity ineluctably unfolded from relatively simple phenomena invested with enormous potential. Sometime long ago in the Protererozoic times, parasitic invasions caused lower evolutionary levels to integrate into higher-level selection. Therefore, we have a multi-level selection problem that ultimately revolves around the question of how natural selection among lower-level units acts to create higher-level units of selection, in which Darwinian competition among replicators ceases to be the foremost force. The first level relinquishes its independence for the benefit of a higher-level cooperative force that is now the criterion of fitness for the new transition in the evolutionary process.     

Attention facilitates multiple stimulus features in parallel in human visual cortex

Successfully locating a dangerous or desirable object within a cluttered visual scene is a commonplace yet highly adaptive skill. In the laboratory, this ability is modeled by visual search experiments in which subjects try to find a target item surrounded by an array of distracting stimuli. Under certain conditions, targets that are distinguishable from distractors by virtue of having a particular combination of shared sensory features (e.g., a particular color and orientation) can be found rapidly regardless of the number of distractors. To explain this highly efficient localization of feature-conjunction targets, "guided search" theories propose that attention is directed in parallel to the individual features that define the target, which then stands out from the distractors because of additive facilitation of its feature signals. Here we recorded frequency-tagged potentials evoked in human visual cortex and found that color and orientation features of target stimuli are indeed facilitated by attention in a parallel and additive manner. This additive feature-enhancement mechanism, reported here for the first time, not only enables rapid guided search but also plays a broader role in directing and sustaining attention to multi-feature objects and keeping them perceptually distinct from background clutter.     

Search efficiency but not response interference affects visual selection in frontal eye field

Two manipulations of a visual search task were used to test the hypothesis that the discrimination of a target from distractors by visually responsive neurons in the frontal eye field (FEF) marks the outcome and conclusion of visual processing instead of saccade preparation. First, search efficiency was reduced by increasing the similarity of the distractors to the target. Second, response interference was introduced by infrequently changing the location of the target in the array. Both manipulations increased reaction time, but only the change in search efficiency affected the time needed to select the target by visually responsive neurons. This result indicates that visually responsive neurons in FEF form an explicit representation of the location of the target in the image.     

Top-Down but Not Bottom-Up Visual Scanning is Affected in Hereditary Pure Cerebellar Ataxia

The aim of this study was to clarify the nature of visual processing deficits caused by cerebellar disorders. We studied the performance of two types of visual search (top-down visual scanning and bottom-up visual scanning) in 18 patients with pure cerebellar types of spinocerebellar degeneration (SCA6: 11; SCA31: 7). The gaze fixation position was recorded with an eye-tracking device while the subjects performed two visual search tasks in which they looked for a target Landolt figure among distractors. In the serial search task, the target was similar to the distractors and the subject had to search for the target by processing each item with top-down visual scanning. In the pop-out search task, the target and distractor were clearly discernible and the visual salience of the target allowed the subjects to detect it by bottom-up visual scanning. The saliency maps clearly showed that the serial search task required top-down visual attention and the pop-out search task required bottom-up visual attention. In the serial search task, the search time to detect the target was significantly longer in SCA patients than in normal subjects, whereas the search time in the pop-out search task was comparable between the two groups. These findings suggested that SCA patients cannot efficiently scan a target using a top-down attentional process, whereas scanning with a bottom-up attentional process is not affected. In the serial search task, the amplitude of saccades was significantly smaller in SCA patients than in normal subjects. The variability of saccade amplitude (saccadic dysmetria), number of re-fixations, and unstable fixation (nystagmus) were larger in SCA patients than in normal subjects, accounting for a substantial proportion of scattered fixations around the items. Saccadic dysmetria, re-fixation, and nystagmus may play important roles in the impaired top-down visual scanning in SCA, hampering precise visual processing of individual items.     

Distractor Interference during a Choice Limb Reaching Task

According to action-centered models of attention, the patterns of distractor interference that emerge in selective reaching tasks are related to the time and effort required to resolve a race for activation between competing target and non-target response producing processes. Previous studies have only used unimanual aiming tasks and, as such, only examined the effects of competition that occurs within a limb. The results of studies using unimanual aiming movements often reveal an “ipsilateral effect” - distractors on the same side of space as the effector cause greater interference than distractors on the opposite side of space. The cost of the competition when response selection is between the limbs has yet to be addressed. Participants in the present study executed reaching movements to 1 of 4 (2 left, 2 right) possible target locations with and without a distractor. Participants made ipsilateral reaches (left hand to left targets, right hand to right targets). In contrast to studies using unimanual aiming movements, a “contralateral effect” was observed; distractors affording responses for the other hand (in contralateral space) caused more interference than distractors affording responses for the same hand. The findings from the present research demonstrate that when certain portions of response planning must be resolved prior to response initiation, distractors that code for that dimension cause the greatest interference.     

Cooperation and conflict in the evolution of individuality. IV. Conflict mediation and evolvability in Volvox carteri

The continued well being of evolutionary individuals (units of selection and evolution) depends upon their evolvability, that is their capacity to generate and evolve adaptations at their level of organization, as well as their longer term capacity for diversifying into more complex evolutionary forms. During a transition from a lower- to higher-level individual, such as the transition between unicellular and multicellular organisms, the evolvability of the lower-level (cells) must be restricted, while the evolvability of the new higher-level unit (multicellular organism) must be enhanced. For these reasons, understanding the factors leading to an evolutionary transition should help us to understand the factors underlying the emergence of evolvability of a new evolutionary unit. Cooperation among lower-level units is fundamental to the origin of new functions in the higher-level unit. Cooperation can produce a new more complex evolutionary unit, with the requisite properties of heritable fitness variations, because cooperation trades fitness from a lower-level (the costs of cooperation) to the higher-level (the benefits for the group). For this reason, the evolution of cooperative interactions helps us to understand the origin of new and higher-levels of fitness and organization. As cooperation creates a new level of fitness, it also creates the opportunity for conflict between levels of selection, as deleterious mutants with differing effects at the two levels arise and spread. This conflict can interfere with the evolvability of the higher-level unit, since the lower and higher-levels of selection will often "disagree" on what adaptations are most beneficial to their respective interests. Mediation of this conflict is essential to the emergence of the new evolutionary unit and to its continued evolvability. As an example, we consider the transition from unicellular to multicellular organisms and study the evolution of an early-sequestered germ-line in terms of its role in mediating conflict between the two levels of selection, the cell and the cell group. We apply our theoretical framework to the evolution of germ/soma differentiation in the green algal group Volvocales. In the most complex member of the group, Volvox carteri, the potential conflicts among lower-level cells as to the "right" to reproduce the higher-level individual (i.e. the colony) have been mediated by restricting immortality and totipotency to the germ-line. However, this mediation, and the evolution of an early segregated germ-line, was achieved by suppressing mitotic and differentiation capabilities in all post-embryonic cells. By handicapping the soma in this way, individuality is ensured, but the solution has affected the long-term evolvability of this lineage. We think that although conflict mediation is pivotal to the emergence of individuality at the higher-level, the way in which the mediation is achieved can greatly affect the longer-term evolvability of the lineage.     

Integration and Disruption Effects of Shape and Texture in Haptic Search

In a search task, where one has to search for the presence of a target among distractors, the target is sometimes easily found, whereas in other searches it is much harder to find. The performance in a search task is influenced by the identity of the target, the identity of the distractors and the differences between the two. In this study, these factors were manipulated by varying the target and distractors in shape (cube or sphere) and roughness (rough or smooth) in a haptic search task. Participants had to grasp a bundle of items and determine as fast as possible whether a predefined target was present or not. It was found that roughness and edges were relatively salient features and the search for the presence of these features was faster than for their absence. If the task was easy, the addition of these features could also disrupt performance, even if they were irrelevant for the search task. Another important finding was that the search for a target that differed in two properties from the distractors was faster than a task with only a single property difference, although this was only found if the two target properties were non-salient. This means that shape and texture can be effectively integrated. Finally, it was found that edges are more beneficial to a search task than disrupting, whereas for roughness this was the other way round.     

On the reorganization of fitness during evolutionary transitions in individuality

The basic problem in an evolutionary transition is to understandhow a group of individuals becomes a new kind of individual,possessing the property of heritable variation in fitness atthe new level of organization. During an evolutionary transition,for example, from single cells to multicellular organisms, thenew higher-level evolutionary unit (multicellular organism)gains its emergent properties by virtue of the interactionsamong lower-level units (cells). We see the formation of cooperativeinteractions among lower-level units as a necessary step inevolutionary transitions; only cooperation transfers fitnessfrom lower levels (costs to group members) to higher levels(benefits to the group). As cooperation creates new levels offitness, it creates the opportunity for conflict between levelsas deleterious mutants arise and spread within the group. Fundamentalto the emergence of a new higher-level unit is the mediationof conflict among lower-level units in favor of the higher-levelunit. The acquisition of heritable variation in fitness at thenew level, via conflict mediation, requires the reorganizationof the basic components of fitness (survival and reproduction)and life-properties (such as immortality and totipotency) aswell as the co-option of lower-level processes for new functionsat the higher level. The way in which the conflicts associatedwith the transition in individuality have been mediated, andfitness and general life-traits have been re-organized, caninfluence the potential for further evolution (i.e., evolvability)of the newly emerged evolutionary individual. We use the volvocaleangreen algal group as a model-system to understand evolutionarytransitions in individuality and to apply and test the theoreticalprinciples presented above. Lastly, we discuss how the differentnotions of individuality stem from the basic properties of fitnessin a multilevel selection context.     

Neuronal correlates of the set-size effect in monkey lateral intraparietal area

It has long been known that the brain is limited in the amount of sensory information that it can process at any given time. A well-known form of capacity limitation in vision is the set-size effect, whereby the time needed to find a target increases in the presence of distractors. The set-size effect implies that inputs from multiple objects interfere with each other, but the loci and mechanisms of this interference are unknown. Here we show that the set-size effect has a neural correlate in competitive visuo-visual interactions in the lateral intraparietal area, an area related to spatial attention and eye movements. Monkeys performed a covert visual search task in which they discriminated the orientation of a visual target surrounded by distractors. Neurons encoded target location, but responses associated with both target and distractors declined as a function of distractor number (set size). Firing rates associated with the target in the receptive field correlated with reaction time both within and across set sizes. The findings suggest that competitive visuo-visual interactions in areas related to spatial attention contribute to capacity limitations in visual searches.     

Active vision and visual activation in area V4

During normal vision, the focus of gaze continually jumps from one important image feature to the next. In this issue of Neuron, Mazer and Gallant analyze neural activity in higher-level visual cortex during this kind of active visual exploration, and they demonstrate a localized enhancement of visual responses that predicts the target of the upcoming eye movement.     

Correlation of space-time ranges in ecological hierarchies of various nature

Relations between characteristic scales of time and space are analyzed for the hierarchical systems of a various nature. The available data fit well to the power relation: [T] = a[L]b, where [T] and [L] are characteristic ranges of time and space, b--scaling exponent, a--conversion coefficient. The spatio-temporal scales of ocean physical and biological (pelagic) processes are closely overlapped. Contrastingly, the scale for terrestrial and benthic ecosystems and their environments differ noticeably. For terrestrial and benthic ecological systems, and also for atmospheric phenomena, the b values significantly less than 1, that indicates a significant coherence of structure-generating processes integrating lower-level hierarchical units to a higher-level entity. For geomorphological structures, both terrestrial and oceanic, the scaling parameters has appeared close to 1 (a "direct transfer" type of generating processes). For plankton systems, which are related with water masses, the b values vary from 1 (processes of direct transfer) up to 2 (random dispersal or diffusion processes). The author attributes this difference to the principle distinctions in dynamic properties of the physical environments for terrestrial (and probably, benthic) and plankton organisms. Finally, for the units (structures or processes) of one and the same organization level, scaling exponents are significantly higher and close to 2 (diffusive dynamics) or more (rigid spatial limitation). Thus, the development of many ecological structures looks dynamically like diffusion or gradual growth, but their putting in the higher-level order (integrity) is a qualitative leap forward and demands appropriate cooperative organizational processes.     

Attentional Switches and Dual-Task Interference

In four experiments, we studied the time course of interference between detection of an oddball orientation target (OT) in an 8-item circular search display, and identification of a letter target (LT) in a central stream of distractor letters. Dual-task performance for different temporal lags between targets was compared to single-task performance. When the LT preceded the OT, dual-task performance levels were reduced at short inter-target intervals of 0 and 166 ms; when the OT preceded the LT, the dual-task interference was unexpectedly stronger and lasted for up to 500 ms. Resource competition due to temporally overlapping target processing cannot account for this result, because the feature search task is easier than the letter identification task, and therefore would have generated less interference when presented first. Two alternative explanations were explored. First, by manipulating the spatial inter-target distance, we investigated to what degree there is a penalty associated with directing the attentional window from a large object (the search display) to a smaller object (the central letter stream). Second, by varying the duration of the OT and subsequent mask, we studied whether the interference was caused by the difficulty of disengaging attention from the search display. Results support this second explanation and thus indicate that switching attention to the letter stream is hampered by the continuing presence of (masked) search display items. This result shows that attentional effects may play a major role in dual-task execution and can easily obscure interference due to other factors such as resource competition.     

Parametric Modeling of Visual Search Efficiency in Real Scenes

How should the efficiency of searching for real objects in real scenes be measured? Traditionally, when searching for artificial targets, e.g., letters or rectangles, among distractors, efficiency is measured by a reaction time (RT) × Set Size function. However, it is not clear whether the set size of real scenes is as effective a parameter for measuring search efficiency as the set size of artificial scenes. The present study investigated search efficiency in real scenes based on a combination of low-level features, e.g., visible size and target-flanker separation factors, and high-level features, e.g., category effect and target template. Visible size refers to the pixel number of visible parts of an object in a scene, whereas separation is defined as the sum of the flank distances from a target to the nearest distractors. During the experiment, observers searched for targets in various urban scenes, using pictures as the target templates. The results indicated that the effect of the set size in real scenes decreased according to the variances of other factors, e.g., visible size and separation. Increasing visible size and separation factors increased search efficiency. Based on these results, an RT × Visible Size × Separation function was proposed. These results suggest that the proposed function is a practicable predictor of search efficiency in real scenes.     

Active gaze control improves optic flow-based segmentation and steering

An observer traversing an environment actively relocates gaze to fixate objects. Evidence suggests that gaze is frequently directed toward the center of an object considered as target but more likely toward the edges of an object that appears as an obstacle. We suggest that this difference in gaze might be motivated by specific patterns of optic flow that are generated by either fixating the center or edge of an object. To support our suggestion we derive an analytical model that shows: Tangentially fixating the outer surface of an obstacle leads to strong flow discontinuities that can be used for flow-based segmentation. Fixation of the target center while gaze and heading are locked without head-, body-, or eye-rotations gives rise to a symmetric expansion flow with its center at the point being approached, which facilitates steering toward a target. We conclude that gaze control incorporates ecological constraints to improve the robustness of steering and collision avoidance by actively generating flows appropriate to solve the task.     

Training Top-Down Attention Improves Performance on a Triple-Conjunction Search Task

Training has been shown to improve perceptual performance on limited sets of stimuli. However, whether training can generally improve top-down biasing of visual search in a target-nonspecific manner remains unknown. We trained subjects over ten days on a visual search task, challenging them with a novel target (top-down goal) on every trial, while bottom-up uncertainty (distribution of distractors) remained constant. We analyzed the changes in saccade statistics and visual behavior over the course of training by recording eye movements as subjects performed the task. Subjects became experts at this task, with twofold increased performance, decreased fixation duration, and stronger tendency to guide gaze toward items with color and spatial frequency (but not necessarily orientation) that resembled the target, suggesting improved general top-down biasing of search.