Gaze behaviour in hereditary prosopagnosia

Prosopagnosia is the inability to recognize someone by the face alone in the absence of sensory or intellectual impairment. In contrast to the acquired form of prosopagnosia we studied the congenital form. Since we could recently show that this form is inherited as a simple monogenic trait we called it hereditary form. To determine whether not only face recognition and neuronal processing but also the perceptual acquisition of facial information is specific to prosopagnosia, we studied the gaze behaviour of four hereditary prosopagnosics in comparison to matched control subjects. This rarely studied form of prosopagnosia ensures that deficits are limited to face recognition. Whereas the control participants focused their gaze on the central facial features, the hereditary prosopagnosics showed a significantly different gaze behaviour. They had a more dispersed gaze and also fixated external facial features. Thus, the face recognition impairment of the hereditary prosopagnosics is reflected in their gaze behaviour.     

Holistic processing impairment can be restricted to faces in acquired prosopagnosia: Evidence from the global/local Navon effect

Previous studies have shown that acquired prosopagnosia is characterized by impairment at holistic/configural processing. However, this view is essentially supported by studies performed with patients whose face recognition difficulties are part of a more general visual (integrative) agnosia. Here, we tested the patient PS, a case of acquired prosopagnosia whose face‐specific recognition difficulties have been related to the inability to process individual faces holistically (absence of inversion, composite, and whole–part effects with faces). Here, we show that in contrast to this impairment, the patient presents with an entirely normal response profile in a Navon hierarchical letter task: she was as fast as normal controls, faster to identify global than local letters, and her sensitivity to global interference during identification of local letters was at least as large as normal observers. These observations indicate that holistic processing as measured with global/local interference in the Navon paradigm is functionally distinct from the ability to perceive an individual face holistically.     

The role of holistic face processing in acquired prosopagnosia: evidence from the composite face effect

Faces are processed more holistically than other objects, and it has been suggested that the loss of holistic face processing causes acquired prosopagnosia. Support for this hypothesis comes from several cases who failed to show holistic face effects as well as the absence of reports of prosopagnosics with unequivocally normal holistic face perception. The current study examines the relationship between holistic face processing and prosopagnosia by testing seven acquired prosopagnosics with the face composite task, a classic measure of holistic face processing. To enhance the robustness of the findings, each prosopagnosic was tested with two versions of the composite task showing upright faces. We also tested an inverted condition to exclude the possibility that more general factors account for composite effects for upright faces. Four of the seven acquired prosopagnosic participants showed consistent upright face composite effects with minimal inverted face composite effects. We conclude that severe face processing deficits can co-occur with intact holistic face processing and that factors other than a loss of holistic processing contribute to the perceptual and recognition deficits in acquired prosopagnosia.     

知觉场理论对面孔知觉年龄偏差效应的解释

使用融合面孔范式和倒置面孔范式来研究面孔知觉的年龄偏差效应,检验知觉场能否作为面孔整体加工的指标,并以此发展年龄偏差的整体加工解释。结果发现：（1）成人和儿童在加工正立面孔时的知觉场均大于加工倒置面孔时的知觉场;（2）在加工正立面孔时,成人加工本年龄面孔比加工他年龄面孔的知觉场更大。上述结果表明：（1）知觉场大小可以作为面孔整体加工的指标,且受面孔朝向的影响;（2）知觉场假设可以解释面孔的年龄偏差效应。     

知觉场理论对面孔知觉年龄偏差效应的解释

使用融合面孔范式和倒置面孔范式来研究面孔知觉的年龄偏差效应,检验知觉场能否作为面孔整体加工的指标,并以此发展年龄偏差的整体加工解释。结果发现：（1）成人和儿童在加工正立面孔时的知觉场均大于加工倒置面孔时的知觉场;（2）在加工正立面孔时,成人加工本年龄面孔比加工他年龄面孔的知觉场更大。上述结果表明：（1）知觉场大小可以作为面孔整体加工的指标,且受面孔朝向的影响;（2）知觉场假设可以解释面孔的年龄偏差效应。     

Dissociation of facial attractiveness and distinctiveness processing in congenital prosopagnosia

According to the influential model of Bruce and Young (1986) socially relevant facial information is processed separately from facial information leading to individual face recognition. In recent years functional imaging has identified a network of distinct occipitotemporal cortex areas for the processing of these two kinds of information. Functionally it is not clear at which processing level the “social” and the “recognition” pathways diverge. The study of subjects with a profound face recognition and learning deficit (congenital prosopagnosia—cPA) promises for a better understanding of this issue. We therefore tested the perception of attractiveness (a cue of prime social importance) and distinctiveness (a facial feature related to recognition) in 14 people with cPA. Although attractiveness ratings were highly consistent with controls, cPA subjects' distinctiveness ratings showed random patterns. This dissociation of normal attractiveness processing and impaired distinctiveness processing in cPA helps to specifies the nature of the impairment in this condition while shedding light on the functional architecture of normal face processing.     

The “parts and wholes” of face recognition: A review of the literature

It has been claimed that faces are recognized as a “whole” rather than by the recognition of individual parts. In a paper published in the Quarterly Journal of Experimental Psychology in 1993, Martha Farah and I attempted to operationalize the holistic claim using the part/whole task. In this task, participants studied a face and then their memory presented in isolation and in the whole face. Consistent with the holistic view, recognition of the part was superior when tested in the whole-face condition compared to when it was tested in isolation. The “whole face” or holistic advantage was not found for faces that were inverted, or scrambled, nor for non-face objects, suggesting that holistic encoding was specific to normal, intact faces. In this paper, we reflect on the part/whole paradigm and how it has contributed to our understanding of what it means to recognize a face as a “whole” stimulus. We describe the value of part/whole task for developing theories of holistic and non-holistic recognition of faces and objects. We discuss the research that has probed the neural substrates of holistic processing in healthy adults and people with prosopagnosia and autism. Finally, we examine how experience shapes holistic face recognition in children and recognition of own- and other-race faces in adults. The goal of this article is to summarize the research on the part/whole task and speculate on how it has informed our understanding of holistic face processing.     

Can generic expertise explain special processing for faces?

Does face recognition involve face-specific cognitive and neural processes ('domain specificity') or do faces only seem special because people have had more experience of individuating them than they have of individuating members of other homogeneous object categories ('the expertise hypothesis')? Here, we summarize new data that test these hypotheses by assessing whether classic face-selective effects - holistic processing, recognition impairments in prosopagnosia and fusiform face area activation - remain face selective in comparison with objects of expertise. We argue that evidence strongly supports domain specificity rather than the expertise hypothesis. We conclude that the crucial social function of face recognition does not reflect merely a general practice phenomenon and that it might be supported by evolved mechanisms (visual or nonvisual) and/or a sensitive period in infancy.     

Individual differences in holistic processing predict face recognition ability

Why do some people recognize faces easily and others frequently make mistakes in recognizing faces? Classic behavioral work has shown that faces are processed in a distinctive holistic manner that is unlike the processing of objects. In the study reported here, we investigated whether individual differences in holistic face processing have a significant influence on face recognition. We found that the magnitude of face-specific recognition accuracy correlated with the extent to which participants processed faces holistically, as indexed by the composite-face effect and the whole-part effect. This association is due to face-specific processing in particular, not to a more general aspect of cognitive processing, such as general intelligence or global attention. This finding provides constraints on computational models of face recognition and may elucidate mechanisms underlying cognitive disorders, such as prosopagnosia and autism, that are associated with deficits in face recognition.     

Neural and genetic foundations of face recognition and prosopagnosia

Faces are of essential importance for human social life. They provide valuable information about the identity, expression, gaze, health, and age of a person. Recent face‐processing models assume highly interconnected neural structures between different temporal, occipital, and frontal brain areas with several feedback loops. A selective deficit in the visual learning and recognition of faces is known as prosopagnosia, which can be found both in acquired and congenital form. Recently, a hereditary sub‐type of congenital prosopagnosia with a very high prevalence rate of 2.5% has been identified. Recent research results show that hereditary prosopagnosia is a clearly circumscribed face‐processing deficit with a characteristic set of clinical symptoms. Comparing face processing of people of prosopagnosia with that of controls can help to develop a more conclusive and integrated model of face processing. Here, we provide a summary of the current state of face processing research. We also describe the different types of prosopagnosia and present the set of typical symptoms found in the hereditary type. Finally, we will discuss the implications for future face recognition research.     

Reduced fixation on the upper area of personally familiar faces following acquired prosopagnosia

Selective impairment of face recognition following brain damage, as in acquired prosopagnosia, may cause a dramatic loss of diagnosticity of the eye area of the face and an increased reliance on the mouth for identification ( Caldara et al., 2005 ). To clarify the nature of this phenomenon, we measured eye fixation patterns in a case of pure prosopagnosia (PS, Rossion et al., 2003 ) during her identification of photographs of personally familiar faces (27 children of her kindergarten). Her age‐matched colleague served as a control. Consistent with previous evidence, the normal control identified the faces within two fixations located just below the eyes (central upper nose). This pattern (location and duration) of fixations remained unchanged even by increasing difficulty by presenting anti‐caricatures of the faces. In contrast, the great majority of the patient's fixations, irrespective of her accuracy, were located on the mouth. Overall, these observations confirm the abnormally reduced processing of the upper area of the face in acquired prosopagnosia. Most importantly, the prosopagnosic patient also fixated the area of the eyes spontaneously in between the first and last fixation, ruling out alternative accounts of her behaviour such as, for example, avoidance or failure to orient attention to the eyes, as observed in autistic or bilateral amygdala patients. Rather, they reinforce our proposal of a high‐level perceptual account ( Caldara et al., 2005 ), according to which acquired prosopagnosic patients have lost the ability to represent multiple elements of an individual face as a perceptual unit (holistic face perception). To identify a given face, they focus very precisely on local features rather than seeing the whole of a face from its diagnostic centre (i.e. just below the eyes). The upper area of the face is particularly less attended to and less relevant for the prosopagnosic patient because it contains multiple features that require normal holistic perception in order to be the most diagnostic region. Consequently, prosopagnosic patients develop a more robust representation of the mouth, a relatively isolated feature in the face that may contain more information than any single element of the upper face area, and is thus sampled repeatedly for resolving ambiguity in the process of identification.     

Prosopagnosia: A reclassification

We report a quantitative investigation of three patients who presented with a profound prosopagnosia. They were tested on a series of tests of face perception, face recognition, and paired associate learning using faces. A patient with marked perceptual difficulties but no difficulty whatever in recognizing faces was tested as a control. The control patient's performance was as bad or worse on the tests of perception of faces, and it is concluded that impaired performance on tests of face perception does not contribute to difficulties in recognizing familiar faces. The major difference between the three prosopagnosic patients was the evidence of covert recognition in two of these cases but not in the third. We use this evidence to argue that the perceptual/mnestic distinction is an inappropriate classification and would suggest instead that the two types may be described in terms either of a disconnection of the face recognition units or of damage to the units themselves.     

What is Overt and what is Covert in Congenital Prosopagnosia?

The term covert recognition refers to recognition without awareness. In the context of face recognition, it refers to the fact that some individuals show behavioural, electrophysiological or autonomic indices of recognition in the absence of overt, conscious recognition. Originally described in cases of people that have lost their ability to overtly recognize faces (acquired prosopagnosia, AP), covert face recognition has more recently also been described in cases of congenital prosopagnosia (CP), who never develop typical overt face recognition skills. The presence of covert processing in a developmental disorder such as CP is a particularly intriguing phenomenon, and its investigation is relevant for a variety of reasons. From a theoretical point of view, it is useful to help shed light on the cognitive and neural underpinnings of face recognition deficits. From a clinical point of view, it has the potential to aid the design of rehabilitation protocols aimed at improving face recognition skills in this population. In the current review we selectively summarize the recent literature on covert face recognition in CP, highlight its main findings, and provide a theoretical interpretation for them.     

The composite face illusion: A whole window into our understanding of holistic face perception

Two identical top halves of a face are perceived as being different when their bottom halves belong to different faces, showing that the parts of a face cannot be perceived independently from the whole face. When this visual illusion is inserted in a matching task, observers make more mistakes and/or are slower at matching identical top face halves aligned with different bottom halves than when the bottom halves are spatially offset: The composite face effect. This composite face paradigm has been used in more than 60 studies that have provided information about the specificity and nature of perceptual integration between facial parts (“holistic face perception”), the impairment of this process in acquired prosopagnosia, its developmental course, temporal dynamics, and neural basis. Following a review of the main contributions made with the paradigm, I explain its rationale and strengths, and discuss its methodological parameters, making a number of proposals for its optimal use and refinement in order to improve our understanding of holistic face perception. Finally, I explain how this standard composite face paradigm is fundamentally different than the application to facial parts of a congruency/interference paradigm that has a long tradition in experimental psychology since Stroop (1935), and which was originally developed to measure attentional and response interference between different representations rather than perceptual integration. Moreover, a version of this congruency/interference paradigm used extensively over the past years with composite faces lacks a baseline measure and has decisional, attentional, and stimulus confounds, making the findings of these studies impossible to interpret in terms of holistic perception. I conclude by encouraging researchers in this field to concentrate fully on the standard composite face paradigm, gaze contingency, and other behavioural measures that can help us take one of the most important challenges of visual perception research: Understanding the neural mechanisms of holistic face perception.     

Normal perception of Mooney faces in developmental prosopagnosia: Evidence from the N170 component and rapid neural adaptation

Individuals with developmental prosopagnosia (DP) have a severe difficulty recognizing the faces of known individuals in the absence of any history of neurological damage. These recognition problems may be linked to selective deficits in the holistic/configural processing of faces. We used two‐tone Mooney images to study the processing of faces versus non‐face objects in DP when it is based on holistic information (or the facial gestalt) in the absence of obvious local cues about facial features. A rapid adaptation procedure was employed for a group of 16 DPs. Naturalistic photographs of upright faces were preceded by upright or inverted Mooney faces or by Mooney houses. DPs showed face‐sensitive N170 components in response to Mooney faces versus houses, and N170 amplitude reductions for inverted as compared to upright Mooney faces. They also showed the typical pattern of N170 adaptation effects, with reduced N170 components when upright naturalistic test faces were preceded by upright Mooney faces, demonstrating that the perception of Mooney and naturalistic faces recruits shared neural populations. Our findings demonstrate that individuals with DP can utilize global information about face configurations for categorical discriminations between faces and non‐face objects, and suggest that face processing deficits emerge primarily at more fine‐grained higher level stages of face perception.     

Limited evidence of individual differences in holistic processing in different versions of the part-whole paradigm

The part-whole paradigm was one of the first measures of holistic processing and it has been used to address several topics in face recognition, including its development, other-race effects, and more recently, whether holistic processing is correlated with face recognition ability. However the task was not designed to measure individual differences and it has produced measurements with low reliability. We created a new holistic processing test designed to measure individual differences based on the part-whole paradigm, the Vanderbilt Part Whole Test (VPWT). Measurements in the part and whole conditions were reliable, but, surprisingly, there was no evidence for reliable individual differences in the part-whole index (how well a person can take advantage of a face part presented within a whole face context compared to the part presented without a whole face) because part and whole conditions were strongly correlated. The same result was obtained in a version of the original part-whole task that was modified to increase its reliability. Controlling for object recognition ability, we found that variance in the whole condition does not predict any additional variance in face recognition over what is already predicted by performance in the part condition.     

Faces are "spatial"--holistic face perception is supported by low spatial frequencies

Faces are perceived holistically, a phenomenon best illustrated when the processing of a face feature is affected by the other features. Here, the authors tested the hypothesis that the holistic perception of a face mainly relies on its low spatial frequencies. Holistic face perception was tested in two classical paradigms: the whole-part advantage (Experiment 1) and the composite face effect (Experiments 2-4). Holistic effects were equally large or larger for low-pass filtered faces as compared to full-spectrum faces and significantly larger than for high-pass filtered faces. The disproportionate composite effect found for low-pass filtered faces was not observed when holistic perception was disrupted by inversion (Experiment 3). Experiment 4 showed that the composite face effect was enhanced only for low spatial frequencies, but not for intermediate spatial frequencies known be critical for face recognition. These findings indicate that holistic face perception is largely supported by low spatial frequencies. They also suggest that holistic processing precedes the analysis of local features during face perception.     

Atypically heterogeneous vertical first fixations to faces in a case series of people with developmental prosopagnosia

ABSTRACT

When people recognize faces, they normally move their eyes so that their first fixation is in the optimal location for efficient perceptual processing. This location is found just below the centre-point between the eyes. This type of attentional bias could be partly innate, but also an inevitable developmental process that aids our ability to recognize faces. We investigated whether a group of people with developmental prosopagnosia would also demonstrate neurotypical first fixation locations when recognizing faces during an eye-tracking task. We found evidence that adults with prosopagnosia had atypically heterogeneous first fixations in comparison to controls. However, differences were limited to the vertical, but not horizontal, plane of the face. We interpret these findings by suggesting that subtle changes to face-based eye movement patterns in developmental prosopagnosia may underpin their face recognition impairments, and suggest future work is still needed to address this possibility.     

Is the Right Anterior Temporal Variant of Prosopagnosia a Form of ‘Associative Prosopagnosia’ or a Form of ‘Multimodal Person Recognition Disorder’?

The construct of associative prosopagnosia is strongly debated for two main reasons. The first is that, according to some authors, even patients with putative forms of associative visual agnosia necessarily present perceptual defects, that are the cause of their recognition impairment. The second is that in patients with right anterior temporal lobe (ATL) lesions (and sparing of the occipital and fusiform face areas), who can present a defect of familiar people recognition, with normal results on tests of face perception, the disorder is often multimodal, affecting voices (and to a lesser extent names) in addition to faces. The present review was prompted by the claim, recently advanced by some authors, that face recognition disorders observed in patients with right ATL lesions should be considered as an associative or amnestic form of prosopagnosia, because in them both face perception and retrieval of personal semantic knowledge from name are spared. In order to check this claim, we surveyed all the cases of patients who satisfied the criteria of associative prosopagnosia reported in the literature, to see if their defect was circumscribed to the visual modality or also affected other channels of people recognition. The review showed that in most patients the study had been limited to the visual modality, but that, when the other modalities of people recognition had been taken into account, the defect was often multimodal, affecting voice (and to a lesser extent name) in addition to face.     

Configural coding of facial expressions: The impact of inversion and photographic negative

In previous research we used the composite paradigm (Young, Hellawell, & Hay, ) to demonstrate that configural cues are important for interpreting facial expressions. However, different configural cues in face perception have been identified, including holistic processing (i.e., perception of facial features as a single gestalt) and second‐order spatial relations (i.e., the spatial relationship between individual features). Previous research has suggested that the composite effect for facial identity operates at the level of holistic encoding. Here we show that the composite effect for facial expression has a similar perceptual basis by using different graphic manipulations (stimulus inversion and photographic negative) in conjunction with the composite paradigm. In relation to Bruce and Young's () functional model of face recognition, a suitable level for the composite effect is a stage of front‐end processing referred to as structural encoding, that is common to both facial identity and facial expression perception.