Developmental prosopagnosia: A case analysis and treatment study

This paper reports a treatment case study focused on face perception impairments designed for AL, an 8-year-old child with prosopagnosia. AL's prosopagnosia was characterized by deficits at the level of structural encoding-that is, he was unable to achieve normal basic perception of faces. This impairment then impacted on all subsequent aspects of familiar- and unfamiliar-face processing. Detailed assessment of feature processing revealed impairments in perception of facial features with a dissociation between relatively good perception of the mouth feature and poor perception of eye and nose features. Interestingly, results also suggested at least partial internal representation of facial features despite long-standing deficits in perception of these features. A treatment programme focused on training in perception, and analysis of facial features and familiar-face naming was conducted. Treatment resulted in excellent face naming for familiar faces, a decreased reliance on nonfacial cues and a reduction in AL's tendency to misidentify unfamiliar faces as family members.     

Face processing in schizophrenia: defining the deficit

BACKGROUND: Abnormalities of face affect naming and face recognition occur in schizophrenia but it is not clear whether the deficits reflect wider underlying impairments of perception, memory, language or executive function. METHOD: Twenty-six patients with schizophrenia were compared with 23 healthy volunteers on neuropsychological tests and tests of face and affect processing. Face and non-face tests were compared at four levels of processing: visuo-spatial perception, recognition memory, language and naming, and executive function. We examined relationships with drug dose, duration of illness and pre-morbid and current IQ. RESULTS: Patients and controls did not differ in estimated pre-morbid IQ but current IQ was 12 points lower in patients. At each level of processing there were correlated deficits of face and non-face processing in the patients that were mostly independent of IQ decline. Impaired face and non-face visuo-spatial function and recognition performance were generally correlated with drug dose. Impairments in naming face emotions were correlated with other non-face naming tasks independently of drug dose. Patients performed less well than controls in classifying faces by emotion while ignoring identity and this was associated with poorer performance in Wisconsin Card Sorting. CONCLUSIONS: The pattern of results suggests that deficits in face processing reflect three wider neuropsychological impairments: a drug-related impairment of visual imagery, and disease-related impairments of semantic retrieval and executive function.     

Normal social cognition in developmental prosopagnosia

Face perception provides information critical to cognitive computations about the social world. This raises the possibility that the development of mechanisms used for social cognition may depend on the presence of normal face perception mechanisms, and this notion partly motivates an aetiological model of autism spectrum disorder (ASD) that suggests that deficits in face perception lead to the social cognition impairments that characterize ASD. To investigate these issues, we examined social cognition in participants with developmental prosopagnosia (DP). A total of 2 male DPs with severe facial identity and facial expression deficits showed no signs of impaired social cognition on three measures. A total of 10 other DPs responded to an inventory measuring autistic traits, and all except one performed normally. These results indicate that social cognition mechanisms can develop normally in the context of developmental face-processing impairments.     

Scan patterns during the processing of facial identity in prosopagnosia

The scan patterns of ocular fixations made by prosopagnosic patients while they attempt to identify faces may provide insights into how they process the information in faces. Contrasts between their scanning of upright versus inverted faces may index the presence of a hypothesized orientation-dependent expert mechanism for processing faces, while contrasts between their scanning of familiar versus novel faces may index the influence of residual facial memories on their search for meaningful facial information. We recorded the eye movements of two prosopagnosics while they viewed faces. One patient, with acquired prosopagnosia from a right occipitotemporal lesion, showed degraded orientation effects but still with a normal distribution of fixations to more salient facial features. However, the dynamics of his global scan patterns were more chaotic for novel faces, suggesting degradation of an internal facial schema, and consistent with other evidence of impaired face configuration perception in this patient. His global scan patterns for famous faces differed from novel faces, suggesting the influence of residual facial memories, as indexed previously by his relatively good imagery for famous faces. The other patient, with a developmental prosopagnosia, showed anomalous orientation effects, abnormal distribution of fixations to less salient regions, and chaotic global scan patterns, in keeping with a more severe loss of face-expert mechanisms. The effects of fame on her scanning were weaker than those in the first subject and non-existent in her global scan patterns. We conclude that scan patterns in prosopagnosia can both reflect the loss of orientation-dependent expert mechanisms and index the covert influence of residual facial memories. In these two subjects the scanning data were consistent with other results from tests of configuration perception, imagery, and covert recognition.     

The role of affect and reasoning in a patient with a delusion of misidentification

Introduction. This study investigated a patient with a delusion of misidentification (DM) resembling a Capgras delusion. Instead of the typical Capgras delusion - the false belief that someone has been replaced by an almost identical impostor - patient MF misidentified his wife as his former business partner. Method. Detailed investigation of MF's face processing, affective response and affect perception, and ability to evaluate, and reject, implausible ideas was undertaken. Results. MF's visual processing of identity, gender, and age of familiar and unknown faces was intact but he was unable to identify the facial expressions of anger, disgust, and fear, or to match faces across expressions. MF also showed a reduced affective responsiveness to his environment, and impaired reasoning ability. Conclusions. We propose that MF's delusion of misidentification resulted from a combination of affective deficits, including impairment of both affective response and affect perception, in addition to an inability to evaluate, and reject, implausible ideas. These deficits, in combination with specific life events at the time of onset of the delusion, may have contributed to the form and content of the delusion. In addition, the results raise the possibility that the processing of face identity and facial expression are not as independent as previously proposed in models of face processing.     

Training of familiar face recognition and visual scan paths for faces in a child with congenital prosopagnosia

In the current report we describe a successful training study aimed at improving recognition of a set of familiar face photographs in K., a 4-year-old girl with congenital prosopagnosia (CP). A detailed assessment of K.'s face-processing skills showed a deficit in structural encoding, most pronounced in the processing of facial features within the face. In addition, eye movement recordings revealed that K.'s scan paths for faces were characterized by a large percentage of fixations directed to areas outside the internal core features (i.e., eyes, nose, and mouth), in particular by poor attendance to the eye region. Following multiple baseline assessments, training focused on teaching K. to reliably recognize a set of familiar face photographs by directing visual attention to specific characteristics of the internal features of each face. The training significantly improved K.'s ability to recognize the target faces, with her performance being flawless immediately after training as well as at a follow-up assessment 1 month later. In addition, eye movement recordings following training showed a significant change in K.'s scan paths, with a significant increase in the percentage of fixations directed to the internal features, particularly the eye region. Encouragingly, not only was the change in scan paths observed for the set of familiar trained faces, but it generalized to a set of faces that was not presented during training. In addition to documenting significant training effects, our study raises the intriguing question of whether abnormal scan paths for faces may be a common factor underlying face recognition impairments in childhood CP, an issue that has not been explored so far.     

Acquired prosopagnosia with spared within-class object recognition but impaired recognition of degraded basic-level objects

We present a new case of acquired prosopagnosia resulting from extensive lesions predominantly in the right occipitotemporal cortex. Functional brain imaging revealed atypical activation of all core face areas in the right hemisphere, with reduced signal difference between faces and objects compared to controls. In contrast, Herschel's lateral occipital complex showed normal activation to objects. Behaviourally, Herschel is severely impaired with the recognition of familiar faces, discrimination between unfamiliar identities, and the perception of facial expression and gender. Notably, his visual recognition deficits are largely restricted to faces, suggesting that the damaged mechanisms are face-specific. He showed normal recognition memory for a wide variety of object classes in several paradigms, normal ability to discriminate between highly similar items within a novel object category, and intact ability to name basic objects (except four-legged animals). Furthermore, Herschel displayed a normal face composite effect and typical global advantage and global interference effects in the Navon task, suggesting spared integration of both face and nonface information. Nevertheless, he failed visual closure tests requiring recognition of basic objects from degraded images. This abnormality in basic object recognition is at odds with his spared within-class recognition and presents a challenge to hierarchical models of object perception.     

Training of familiar face recognition and visual scan paths for faces in a child with congenital prosopagnosia

In the current report we describe a successful training study aimed at improving recognition of a set of familiar face photographs in K., a 4-year-old girl with congenital prosopagnosia (CP). A detailed assessment of K.'s face-processing skills showed a deficit in structural encoding, most pronounced in the processing of facial features within the face. In addition, eye movement recordings revealed that K.'s scan paths for faces were characterized by a large percentage of fixations directed to areas outside the internal core features (i.e., eyes, nose, and mouth), in particular by poor attendance to the eye region. Following multiple baseline assessments, training focused on teaching K. to reliably recognize a set of familiar face photographs by directing visual attention to specific characteristics of the internal features of each face. The training significantly improved K.'s ability to recognize the target faces, with her performance being flawless immediately after training as well as at a follow-up assessment 1 month later. In addition, eye movement recordings following training showed a significant change in K.'s scan paths, with a significant increase in the percentage of fixations directed to the internal features, particularly the eye region. Encouragingly, not only was the change in scan paths observed for the set of familiar trained faces, but it generalized to a set of faces that was not presented during training. In addition to documenting significant training effects, our study raises the intriguing question of whether abnormal scan paths for faces may be a common factor underlying face recognition impairments in childhood CP, an issue that has not been explored so far.     

Configuration perception and face memory,and face context effects in developmental prosopagnosia

This study addresses two central and controversial issues in developmental prosopagnosia (DP), configuration- versus feature-based face processing and the influence of affective information from either facial or bodily expressions on face recognition. A sample of 10 DPs and 10 controls were tested with a previously developed face and object recognition and memory battery (Facial Expressive Action Stimulus Test, FEAST), a task measuring the influence of emotional faces and bodies on face identity matching (Face–Body Compound task), and an emotionally expressive face memory task (Emotional Face Memory task, FaMe-E). We show that DPs were impaired in upright, but not inverted, face matching but they performed at the level of controls on part-to-whole matching. Second, DPs showed impaired memory for both neutral and emotional faces and scored within the normal range on the Face–Body Compound task. Third, configural perception but not feature-based processing was significantly associated with memory performance. Taken together the results indicate that DPs have a deficit in configural processing at the perception stage that may underlie the memory impairment.     

Face inversion superiority in a case of prosopagnosia following congenital brain abnormalities: What can it tell us about the specificity and origin of face-processing mechanisms?

In the current study we describe J.M., a 15-year-old boy with a history of congenital brain abnormalities and concomitant visual-processing impairments. J.M.'s most prominent deficit is his impaired face recognition, but formal testing also revealed deficits in other domains of visual processing. One aspect that emerged from J.M.'s visual-processing assessment was a tendency to focus on local features and to rely on them for the encoding and identification of visual stimuli including geometric figures, objects, words, and inverted faces. In spite of this general tendency, he was impaired on tasks requiring the encoding of local features in upright faces. Moreover, his ability to distinguish between features in upright faces was significantly worse than that for inverted faces, the opposite pattern to that typically found in normal participants. What is it that keeps J.M. from applying his otherwise intact feature-based processing to upright faces? As proposed in previous reports of face inversion superiority in individuals with acquired face recognition impairments, we suggest that J.M.'s “inverted-face inversion effect” speaks for a specialized cognitive system that is mandatorily engaged by upright (but not inverted) faces, even when it is impaired and therefore maladaptive. In addition, since J.M. suffered from congenital brain abnormalities affecting the normal development of his face-processing skills, his performance suggests that specialized and mandatorily activated face-processing mechanisms are not entirely experience dependent, and that they can remain modular during development even if they don't function properly and are therefore maladaptive.     

Face recognition without awareness

PH has been completely unable to recognise faces since sustaining a closed head injury some four years ago, but can recognise familiar people from their names. His performance on face processing tasks is, however, comparable to that of normal subjects if explicit recognition is not required. Thus he can make same/different identity judgements more quickly for familiar than unfamiliar face photographs, and faster matching of familiar faces is only found for identity matches involving the face's internal features. When making semantic categorisation decisions to printed names he shows interference from distractor faces belonging to an incorrect category, even when the faces in each category are matched on physical appearance. When learning to associate the occupation or the name with photographs of faces, his performance is better with true (face and person's actual name or occupation) than untrue (face and another person's name or occupation) pairings. Covert recognition can also be demonstrated for faces of people PH has only met since his accident. These findings show that in prosopagnosia, much of the processing of familiar faces can remain intact despite absence of awareness that recognition has occurred.     

The contribution of the fusiform gyrus and superior temporal sulcus in processing facial attractiveness: neuropsychological and neuroimaging evidence

Current cognitive models suggest that the processing of dynamic facial attributes, including social signals such as gaze direction and facial expression, involves the superior temporal sulcus, whereas the processing of invariant facial structure such as the individuals' identity involves the fusiform face area. Where facial attractiveness, a social signal that may emerge from invariant facial structure, is processed within this dual-route model of face perception is uncertain. Here, we present two studies. First, we investigated the explicit judgments of facial attractiveness and attractiveness-motivated behavior in patients with acquired prosopagnosia, a deficit in familiar face recognition usually associated with damage to medial occipitotemporal cortex. We found that both abilities were impaired in these patients, with some weak residual ability for attractiveness judgments found only in those patients with unilateral right occipitotemporal or bilateral anterior temporal lesions. Importantly, deficits in attractiveness perception correlated with the severity of the face recognition deficit. Second, we performed a functional magnetic resonance imaging study in healthy subjects that included an implicit and explicit processing of facial attractiveness. We found increased neural activity when explicitly judging facial attractiveness within a number of cortical regions including the fusiform face area, but not the superior temporal sulcus, indicating a potential contribution of the fusiform face area to this judgment. Thus, converging neuropsychological and neuroimaging evidence points to a critical role of the inferior occipitotemporal cortex in the processing of facial attractiveness.     

Topographic processing in developmental prosopagnosia: Preserved perception but impaired memory of scenes

Anecdotal evidence suggests a relation between impaired spatial (navigational) processing and developmental prosopagnosia. To address this formally, we tested two aspects of topographic processing – that is, perception and memory of mountain landscapes shown from different viewpoints. Participants included nine individuals with developmental prosopagnosia and 18 matched controls. The group with developmental prosopagnosia had no difficulty with topographic perception, but was reliably poorer in the retention of topographic information. Additional testing revealed that this did not reflect a general deficit in visual processing or visual short-term memory. Interestingly, a classical dissociation could be demonstrated between impaired face memory and preserved topographic memory in two developmental prosopagnosics. We conclude that impairments in topographic memory tend to co-occur with developmental prosopagnosia, although the underlying functions are likely to be independent.     

Perceptual separability of featural and configural information in congenital prosopagnosia

The deficit in face recognition in individuals with prosopagnosia has often been attributed to an underlying impairment in holistic processing. Exactly what constitutes holistic processing has remained controversial, however. Here, we compare how configural information and featural information interact during face processing in a group of individuals with congenital prosopagnosia (CP) and matched controls. We adopted Amishav and Kimchi's version of Garner's speeded classification task, in which observers classify upright faces based on configural (intereyes and nose–mouth spacing) or featural (shape of eyes, nose, and mouth) information while the other dimension remains constant or varied randomly. We replicated the finding that normal observers evince symmetric Garner interference—failure to selectively attend to features without being influenced by irrelevant variation in configuration, and vice versa—indicating that featural and configural information are integral in normal face processing. In contrast, the CPs showed no Garner interference: They were able to attend to configural information without interference from irrelevant variation in featural information, and they were able to attend to featural information without interference from irrelevant variation in configural information. The absence of Garner interference in CP provides strong evidence that featural information and configural information are perceptually separable in CP's face processing. These findings indicate that CPs do not perceive faces holistically; rather, they process featural and configural information independently.     

The Philadelphia Face Perception Battery.

The Philadelphia Face Perception Battery (PFPB) tests four aspects of face perception: discrimination of facial similarity, attractiveness, gender, and age. Calibration with 116 neurologically intact subjects yielded average performance of approximately 90%. Across subjects, there was a low correlation (<0.22) in performance between the tests (with the exception of the attractiveness and age discrimination tests) suggesting that the tests measure independent aspects of face perception. There were modest effects of subject demographic factors upon performance, and test-retest reliability scores (between 0.37 and 0.75) were comparable to other neuropsychological batteries. Modification of the stimuli to obscure internal facial features lowered performance on the age, gender, and attractiveness discrimination tests between 2 and 4 standard deviations. The clinical sensitivity of the battery was demonstrated by testing a patient with acquired prosopagnosia. She showed performance impairments of between 2 and 4 standard deviations on all sub-tests. The PFPB is freely available for non-commercial use.     

Electrophysiological studies of face processing in developmental prosopagnosia: Neuropsychological and neurodevelopmental perspectives

People with developmental prosopagnosia (DP) show severe face-recognition deficits that typically emerge during childhood without history of neurological damage. We review findings from recent event-related brain potential (ERP) studies of face perception and face recognition in DP. The generic face-sensitivity of the N170 component is present in most DPs, suggesting rapid category-selective streaming of facial information. In contrast, DPs show atypical N170 face inversion effects, indicative of impaired structural encoding, specifically for upright faces. In line with neurodevelopmental accounts of DP, these effects are similar to those observed for other developmental disorders, as well as for younger children and older adults. Identity-sensitive ERP components (N250, P600f) triggered during successful face recognition are similar for DPs and control participants, indicating that the same mechanisms are active in both groups. The presence of covert face-recognition effects for the N250 component suggests that visual face memory and semantic memory can become disconnected in some individuals with DP. The implications of these results for neuropsychological and neurodevelopmental perspectives on DP are discussed.     

Recognition of Facial Expressions: Selective Impairment of Specific Emotions in Huntington's Disease

Recognition of facial expressions of basic emotions was investigated in HL and UJ, two people with Huntington's disease who showed little evidence of general cognitive deterioration. No impairments were found in tests of the perception of age, sex, familiar face identity, unfamiliar face identity, and gaze direction, indicating adequate processing of the face as a physical stimulus. Computer-interpolated ("morphed") images of facial expressions of basic emotions were used to demonstrate deficits in the recognition of disgust and fear for UJ. HL also showed a deficit in the recognition of disgust, and was not very adept (but not significantly impaired) at recognising fear. Other basic emotions (happiness, surprise, sadness, anger) were recognised atnormal levels of performance by HL and UJ. These results show that impairments of emotion recognition can be circumscribed; affecting some emotions more than others, and occurring in people who do not show pronounced perceptual or intellectual deterioration. Questionnaires examining self-assessed emotion indicated normal experience of anger by HL and UJ, but possible abnormalities for disgust and fear. The processes involved in recognising other people's emotions may therefore be linked to those involved in experiencing emotion, and the basic emotions of fear and disgust may have separable neural substrates.     

METHODOLOGICAL ISSUES CONFRONTING PET AND fMRI STUDIES OF COGNITIVE FUNCTION

We report data from a patient, NE, who after surviving encephalitis made misidentification responses to faces known to her premorbidly. NE frequently mistook one famous person for another, one relative for another, and, under some conditions, believed that a picture of a famous person actually depicted one of her relatives. Unlike previously reported patients who have misidentified faces, NE (1) performed reasonably well on tests of facial perception, (2) showed no obvious executive deficits in tests of frontal lobe function, and (3) showed an ability to constrain her misidentification responses in certain situations. A cognitive neuropsychological investigation revealed that NE was able to judge misidentified faces as familiar but failed to access precise semantic information. There were also semantic deficits when knowledge of people was probed through nonvisual modalities—for example, when naming people from definition. We argue that a semantic, as opposed to executive, deficit plays the major (though probably not sole) role in NE's misidentification responses, and we consider how the inter‐active activation model of face recognition (Burton, Bruce, &; Johnston, 1990) can account for such disorders of person recognition more comprehensively than the Bruce and Young (1986) model.     

Understanding the nature of face processing impairment in autism: insights from behavioral and electrophysiological studies

This article reviews behavioral and electrophysiological studies of face processing and discusses hypotheses for understanding the nature of face processing impairments in autism. Based on results of behavioral studies, this study demonstrates that individuals with autism have impaired face discrimination and recognition and use atypical strategies for processing faces characterized by reduced attention to the eyes and piecemeal rather than configural strategies. Based on results of electrophysiological studies, this article concludes that face processing impairments are present early in autism, by 3 years of age. Such studies have detected abnormalities in both early (N170 reflecting structural encoding) and late (NC reflecting recognition memory) stages of face processing. Event-related potential studies of young children and adults with autism have found slower speed of processing of faces, a failure to show the expected speed advantage of processing faces versus nonface stimuli, and atypical scalp topography suggesting abnormal cortical specialization for face processing. Other electrophysiological studies have suggested that autism is associated with early and late stage processing impairments of facial expressions of emotion (fear) and decreased perceptual binding as reflected in reduced gamma during face processing. This article describes two types of hypotheses-cognitive/perceptual and motivational/affective--that offer frameworks for understanding the nature of face processing impairments in autism. This article discusses implications for intervention.