Discrimination of faces and houses by rhesus monkeys: the role of stimulus expertise and rotation angle

The face inversion effect, or impaired recognition of upside down compared to upright faces, is used as a marker for the configural processing of faces in primates. The inversion effect in humans and chimpanzees is strongest for categories of stimuli for which subjects have considerable expertise, primarily conspecifics’ faces. Moreover, discrimination performance decreases linearly as faces are incrementally rotated from upright to inverted. This suggests that rotated faces must be transformed, or normalized back into their most typical viewpoint before configural processing can ensue, and the greater the required normalization, the greater the likelihood of errors resulting. Previous studies in our lab have demonstrated a general face inversion effect in rhesus monkeys that was not influenced by expertise. Therefore, the present study examined the influence of rotation angle on the visual perception of face and nonface stimuli that varied in their level of expertise to further delineate the processes underlying the inversion effect in rhesus monkeys. Five subjects discriminated images in five orientation angles. Results showed significant linear impairments for all stimulus categories, including houses. However, compared to the upright images, only rhesus faces resulted in worse performance at rotation angles greater than 45°, suggesting stronger configural processing for stimuli for which subjects had the greatest expertise.     

Perceptual specialization and configural face processing in infancy

Adults’ face processing expertise includes sensitivity to second-order configural information (spatial relations among features such as distance between eyes). Prior research indicates that infants process this information in female faces. In the current experiments, 9-month-olds discriminated spacing changes in upright human male and monkey faces but not in inverted faces. However, they failed to process matching changes in upright house stimuli. A similar pattern of performance was exhibited by 5-month-olds. Thus, 5- and 9-month-olds exhibited specialization by processing configural information in upright primate faces but not in houses or inverted faces. This finding suggests that, even early in life, infants treat faces in a special manner by responding to changes in configural information more readily in faces than in non-face stimuli. However, previously reported differences in infants’ processing of human versus monkey faces at 9 months of age (but not at younger ages), which have been associated with perceptual narrowing, were not evident in the current study. Thus, perceptual narrowing is not absolute in the sense of loss of the ability to process information from other species’ faces at older ages.     

How the Thatcher illusion reveals evolutionary differences in the face processing of primates

Face recognition in humans is a complex cognitive skill that requires sensitivity to unique configurations of eyes, mouth, and other facial features. The Thatcher illusion has been used to demonstrate the importance of orientation when processing configural information within faces. Transforming an upright face so that the eyes and mouth are inverted renders the face grotesque; however, when this “Thatcherized” face is inverted, the effect disappears. Due to the use of primate models in social cognition research, it is important to determine the extent to which specialized cognitive functions like face processing occur across species. To date, the Thatcher illusion has been explored in only a few species with mixed results. Here, we used computerized tasks to examine whether nonhuman primates perceive the Thatcher illusion. Chimpanzees and rhesus monkeys were required to discriminate between Thatcherized and unaltered faces presented upright and inverted. Our results confirm that chimpanzees perceived the Thatcher illusion, but rhesus monkeys did not, suggesting species differences in the importance of configural information in face processing. Three further experiments were conducted to understand why our results differed from previously published accounts of the Thatcher illusion in rhesus monkeys.     

Facial perception of conspecifics: chimpanzees (Pan troglodytes) preferentially attend to proper orientation and open eyes

This paper reports on the use of an eye-tracking technique to examine how chimpanzees look at facial photographs of conspecifics. Six chimpanzees viewed a sequence of pictures presented on a monitor while their eye movements were measured by an eye tracker. The pictures presented conspecific faces with open or closed eyes in an upright or inverted orientation in a frame. The results demonstrated that chimpanzees looked at the eyes, nose, and mouth more frequently than would be expected on the basis of random scanning of faces. More specifically, they looked at the eyes longer than they looked at the nose and mouth when photographs of upright faces with open eyes were presented, suggesting that particular attention to the eyes represents a spontaneous face-scanning strategy shared among monkeys, apes, and humans. In contrast to the results obtained for upright faces with open eyes, the viewing times for the eyes, nose, and mouth of inverted faces with open eyes did not differ from one another. The viewing times for the eyes, nose, and mouth of faces with closed eyes did not differ when faces with closed eyes were presented in either an upright or inverted orientation. These results suggest the possibility that open eyes play an important role in the configural processing of faces and that chimpanzees perceive and process open and closed eyes differently.     

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.     

Perceptual integrality of componential and configural information in faces

The relative contribution of componential and configural information to face perception is controversial. We addressed this issue in the present study by examining how componential information and configural information interact during face processing, using Garner’s (1974) speeded classification paradigm. When classifying upright faces varying in components (eyes, nose, and mouth) and configural information (intereyes and nose-mouth spacing), observers could not selectively attend to components without being influenced by irrelevant variation in configural information, and vice versa, indicating that componential information and configural information are integral in upright face processing. Performance with inverted faces showed selective attention to components but not to configural information, implying dominance of componential information in processing inverted faces. When faces varied only in components, selective attention to different components was observed in upright and inverted faces, indicating that facial components are perceptually separable. These results provide strong evidence that integrality of componential and configural information, rather than the relative dominance of either, is the hallmark of upright face perception.     

The face inversion effect—Parts and wholes: Individual features and their configuration

The face inversion effect (FIE) is a reduction in recognition performance for inverted faces (compared to upright faces) that is greater than that typically observed with other stimulus types (e.g., houses). The work of Diamond and Carey, suggests that a special type of configural information, “second-order relational information” is critical in generating this inversion effect. However, Tanaka and Farah concluded that greater reliance on second-order relational information did not directly result in greater sensitivity to inversion, and they suggested that the FIE is not entirely due to a reliance on this type of configural information. A more recent review by McKone and Yovel provides a meta-analysis that makes a similar point. In this paper, we investigated the contributions made by configural and featural information to the FIE. Experiments 1a and1b investigated the link between configural information and the FIE. Remarkably, Experiment 1b showed that disruption of all configural information of the type considered in Diamond and Carey's analysis (both first and second order) was effective in reducing recognition performance, but did not significantly impact on the FIE. Experiments 2 and 3 revealed that face processing is affected by the orientation of individual features and that this plays a major role in producing the FIE. The FIE was only completely eliminated when we disrupted the single feature orientation information in addition to the configural information, by using a new type of transformation similar to Thatcherizing our sets of scrambled faces. We conclude by noting that our results for scrambled faces are consistent with an account that has recognition performance entirely determined by the proportion of upright facial features within a stimulus, and that any ability to make use of the spatial configuration of these features seems to benefit upright and inverted normal faces alike.     

Remembering parts and wholes: Configural processing in face recollection

In two experiments, we examined the role of configural processing on states of awareness in face recognition. Configural processing was manipulated by presenting upright and inverted faces during study and test. After studying facial photographs of humans (Experiment 1) and horses (Experiment 2), participants provided a remember/know judgement for each recognised test face. In both experiments, disrupted configural processing had selective effects on states of awareness, so that inversion reduced remember, but not know, responses. Experiment 2 revealed disproportionate inversion effects in that the difference in remember responses between upright and inverted items was significant for human faces but not horses. These findings suggest that configural processing facilitates explicit recollection by providing a distinctive combination of nonsalient event attributes.     

Effect of inversion on the recognition of external and internal facial features

The purpose of the present study was to find out whether inversion affects recognition of external and internal facial features. 24 participants matched, under two experimental conditions (pair and multiple-choice matchings), upright target faces with three categories of facial test stimuli: full faces, external features and internal features, which were presented in either upright or inverted orientations. Data analysis showed that matching of facial stimuli was faster, more accurate and more consistent under upright than under inverted orientations for all stimulus categories; mostly for full faces, and least for internal features. As a rule, there were no speed-accuracy trade-offs. Implications of the data for accounts of the inversion effect in face recognition in terms of a shift from configurational to componential processing were discussed.     

面孔加工的结构编码阶段异族效应的加工方式： ERPs研究

实验采用事件相关电位（ERPs）技术,以大学生为被试,运用非洲、欧洲、亚洲三个不同种族的面孔照片,探究异族效应与加工方式的关系。行为实验结果显示,被试对非洲面孔的反应时快于欧洲面孔,且两者均快于亚洲面孔。ERP研究结果显示,亚洲面孔的N170波幅显著小于非洲和欧洲面孔的波幅,后两者的N170波幅没有差异,而且亚洲面孔的倒置效应最大。研究结果说明相对于异族面孔,本族面孔更多地使用构型编码的加工方式,且N170成分表现出右半球优势。     

Emotional context at learning systematically biases memory for facial information

Emotion influences memory in many ways. For example, when a mood-dependent processing shift is operative, happy moods promote global processing and sad moods direct attention to local features of complex visual stimuli. We hypothesized that an emotional context associated with to-be-learned facial stimuli could preferentially promote global or local processing. At learning, faces with neutral expressions were paired with a narrative providing either a happy or a sad context. At test, faces were presented in an upright or inverted orientation, emphasizing configural or analytical processing, respectively. A recognition advantage was found for upright faces learned in happy contexts relative to those in sad contexts, whereas recognition was better for inverted faces learned in sad contexts than for those in happy contexts. We thus infer that a positive emotional context prompted more effective storage of holistic, configural, or global facial information, whereas a negative emotional context prompted relatively more effective storage of local or feature-based facial information     

Multiple perceptual strategies used by macaque monkeys for face recognition

Successful integration of individuals in macaque societies suggests that monkeys use fast and efficient perceptual mechanisms to discriminate between conspecifics. Humans and great apes use primarily holistic and configural, but also feature-based, processing for face recognition. The relative contribution of these processes to face recognition in monkeys is not known. We measured face recognition in three monkeys performing a visual paired comparison task. Monkey and humans faces were (1) axially rotated, (2) inverted, (3) high-pass filtered, and (4) low-pass filtered to isolate different face processing strategies. The amount of time spent looking at the eyes, mouth, and other facial features was compared across monkey and human faces for each type of stimulus manipulation. For all monkeys, face recognition, expressed as novelty preference, was intact for monkey faces that were axially rotated or spatially filtered and was supported in general by preferential looking at the eyes, but was impaired for inverted faces in two of the three monkeys. Axially rotated, upright human faces with a full range of spatial frequencies were also recognized, however, the distribution of time spent exploring each facial feature was significantly different compared to monkey faces. No novelty preference, and hence no inferred recognition, was observed for inverted or low-pass filtered human faces. High-pass filtered human faces were recognized, however, the looking pattern on facial features deviated from the pattern observed for monkey faces. Taken together these results indicate large differences in recognition success and in perceptual strategies used by monkeys to recognize humans versus conspecifics. Monkeys use both second-order configural and feature-based processing to recognize the faces of conspecifics, but they use primarily feature-based strategies to recognize human faces.     

Perception of novel faces: the parts have it!

It has been suggested that, as a result of expertise, configural information plays a predominant role in face processing. We investigated this idea using novel and learned faces. In experiment 1, sixteen participants matched two subsequently presented blurred or scrambled faces, which could be either upright or inverted, in a sequential same -different matching task. By means of blurring, featural information is hampered, whilst scrambling disrupts configural information. Each face was unfamiliar to the participants and was presented for 1000 ms. An ANOVA on the d' values revealed a significant advantage for scrambled faces. In experiment 2, fourteen participants were tested with the same design, except that the second face was always intact. Again, the ANOVA on the d' values revealed a significant advantage for scrambled faces. In experiment 3 half of the faces were learned in a familiarisation block prior to the experiment. The ANOVA of these d' values revealed a significant interaction of familiarity and condition, showing that blurred stimuli were better recognised when the faces were familiar. These results suggest that recognition of novel faces, compared to learned faces, relies relatively more on the processing of featural information. In the course of familiarisation the importance of configural information increases.     

Isolating the special component of face recognition: peripheral identification and a Mooney face

A previous finding argues that, for faces, configural (holistic) processing can operate even in the complete absence of part-based contributions to recognition. Here, this result is confirmed using 2 methods. In both, recognition of inverted faces (parts only) was removed altogether (chance identification of faces in the periphery; no perception of a particularly hard-to-see Mooney face). Recognition of upright faces (configural plus parts), however, remained good. The simplicity of these new "isolation" techniques makes them ideal for (a) assessing configural processing in specialist populations (e.g., children, object experts) and (b) exploring properties of configural processing for faces in detail. As an example of the latter, orientation tuning was tested. Results argue against models in which faces are rotated to upright prior to identification.     

Physical and perceptual accuracy of upright and inverted face drawings

This study considers the conception that drawing or copying a face that is vertically inverted will improve the accuracy of the drawing by preventing holistic interference. We used a novel parameterized face space both for generating face stimuli and for measuring the physical accuracy of drawings. One group of participants (the artists) were asked to draw 16 parameterized faces (eight upright and eight inverted). We computed two physical measures of accuracy by comparing the face-space representation of each drawing to the original face. A second and third group of participants (the raters) compared the similarity between each original face and each pair of drawings of that face (one upright and one inverted per artist). For the second group, all faces were presented upright; for the third group, all faces were presented inverted. Our results showed that upright drawings were more accurate than inverted drawings, both in terms of the physical face-space measure and in terms of the perceptual judgments for both orientations. Our data suggest that holistic processing may aid rather than hinder face drawing accuracy.     

The role of eyes in early face processing: a rapid adaptation study of the inversion effect

The current study employed a rapid adaptation procedure to test the neuronal mechanisms of the face inversion effect (FIE) on the early face-sensitive event-related potential (ERP) component N170. Five categories of face-related stimuli (isolated eyes, isolated mouths, eyeless faces, mouthless faces, and full faces) and houses were presented in upright and inverted orientations as adaptors for inverted full face test stimuli. Strong adaptation was found for all face-related stimuli except mouths. The adaptation effect was larger for inverted than upright stimuli, but only when eyes were present. These results underline an important role of eyes in early face processing. A mechanism of eye-dependent orientation sensitivity during the structural encoding stage of faces is proposed.     

An inversion effect modified by expertise in capuchin monkeys

The face inversion effect may be defined as the general impairment in recognition that occurs when faces are rotated 180°. This phenomenon seems particularly strong for faces as opposed to other objects and is often used as a marker of a specialized face-processing mechanism. Four brown capuchin monkeys (Cebus apella) were tested on their ability to discriminate several classes of facial and non-facial stimuli presented in both their upright and inverted orientations in an oddity task. Results revealed significantly better performance on upright than inverted presentations of capuchin and human face stimuli, but not on chimpanzee faces or automobiles. These data support previous studies in humans and other primates suggesting that the inversion effect occurs for stimuli for which subjects have developed an expertise.     

How dogs scan familiar and inverted faces: an eye movement study

Faces play an important role in communication and identity recognition in social animals. Domestic dogs often respond to human facial cues, but their face processing is weakly understood. In this study, facial inversion effect (deficits in face processing when the image is turned upside down) and responses to personal familiarity were tested using eye movement tracking. A total of 23 pet dogs and eight kennel dogs were compared to establish the effects of life experiences on their scanning behavior. All dogs preferred conspecific faces and showed great interest in the eye area, suggesting that they perceived images representing faces. Dogs fixated at the upright faces as long as the inverted faces, but the eye area of upright faces gathered longer total duration and greater relative fixation duration than the eye area of inverted stimuli, regardless of the species (dog or human) shown in the image. Personally, familiar faces and eyes attracted more fixations than the strange ones, suggesting that dogs are likely to recognize conspecific and human faces in photographs. The results imply that face scanning in dogs is guided not only by the physical properties of images, but also by semantic factors. In conclusion, in a free-viewing task, dogs seem to target their fixations at naturally salient and familiar items. Facial images were generally more attractive for pet dogs than kennel dogs, but living environment did not affect conspecific preference or inversion and familiarity responses, suggesting that the basic mechanisms of face processing in dogs could be hardwired or might develop under limited exposure.     

Internal feature saliency as a marker of familiarity and configural processing

Two experiments that explore the internal feature advantage (IFA) in familiar face processing are reported. The IFA involves more efficient processing of internal features for familiar faces over unfamiliar ones. Experiment 1 examined the possibility of a configural basis for this effect through use of a matching task for familiar and unfamiliar faces presented both upright and upside-down. Results revealed the predicted IFA for familiar faces when stimuli were upright, but this was removed when stimuli were inverted. Experiment 2 examined the degree of training required before the IFA was demonstrated. Latency results revealed that whilst 90–180 s of exposure was sufficient to generate an IFA of intermediate magnitude, 180–270 s of exposure was required before the IFA was equivalent to that demonstrated for a familiar face. Taken together, these results offer three conclusions: First, the IFA is reaffirmed as an objective indicator of familiarity; second, the IFA is seen to rest on configural processing; and finally, the development of the IFA with familiarity indicates a development of configural processing with familiarity. As such, insight is gained as to the type of processing changes that occur as familiarity is gradually acquired.     

Processing style and person recognition: Exploring the face inversion effect

It has frequently been reported that recognition performance is impaired when faces are presented in an inverted rather than upright orientation, a phenomenon termed the face inversion effect (FIE). Extending previous work on this topic, the current investigation explored whether individual differences in global precedence—the propensity to process nonfacial stimuli in a configural manner—impacts memory for faces. Based on performance on the Navon letter-classification task, two experimental groups were created that differed in relative global precedence (i.e., strong global precedence [SGP] and weak global precedence [WGP]). In a subsequent face-recognition task, results revealed that while both groups demonstrated a reliable FIE, this effect was attenuated among participants displaying WGP. These findings suggest that individual differences in general processing style modulate face recognition.