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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

Self and Social Regulation: Social Interaction and the Development of Social Understanding and Executive Functions,by B. W. Sokol,U. Miller,J. I. M. Carpendale,A. R. Young,and G. Iarocci

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.     

Are faces special? A case of pure prosopagnosia

The ability to recognize individual faces is of crucial social importance for humans and evolutionarily necessary for survival. Consequently, faces may be "special" stimuli, for which we have developed unique modular perceptual and recognition processes. Some of the strongest evidence for face processing being modular comes from cases of prosopagnosia, where patients are unable to recognize faces whilst retaining the ability to recognize other objects. Here we present the case of an acquired prosopagnosic whose poor recognition was linked to a perceptual impairment in face processing. Despite this, she had intact object recognition, even at a subordinate level. She also showed a normal ability to learn and to generalize learning of nonfacial exemplars differing in the nature and arrangement of their parts, along with impaired learning and generalization of facial exemplars. The case provides evidence for modular perceptual processes for faces.     

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.     

Electrophysiological correlates of facial configuration and audio�Cvisual congruency: evidence that face processing is a visual rather than a multisensory task

Behavioural, neuroimaging and lesion studies show that face processing has a special role in human perception. The purpose of this EEG study was to explore whether auditory information influences visual face perception. We employed a 2?×?2 factorial design and presented subjects with visual stimuli that could be cartoon faces or scrambled faces where size changes of one of the components, the mouth in the face condition, was either congruent or incongruent with the amplitude modulation of a simultaneously presented auditory signal. Our data show a significant main effect for signal congruence at an ERP peak around 135?ms and a significant main effect of face configuration at around 200?ms. The timing and scalp topology of both effects corresponds well to previously reported data on the integration of non-redundant audio-visual stimuli and face-selective processing. Our analysis did not show any significant statistical interactions. This double disassociation suggests that the early component, at 135?ms, is sensitive to auditory-visual congruency but not to facial configuration and that the later component is sensitive to facial configuration but not to AV congruency. We conclude that facial configurational processing is not influenced by the congruence of simultaneous auditory signals and is independent from featural processing where we see evidence for multisensory integration.     

Could dynamic attractors explain associative prosopagnosia?

Prosopagnosia is one of the many forms of visual associative agnosia, in which familiar faces lose their distinctive association. In the case of prosopagnosia, the ability to recognize familiar faces is lost, due to lesions in the medial occipitotemporal region. In "associative" prosopagnosia, the perceptual system seems adequate to allow for recognition, yet recognition cannot take place. Our hypothesis is that a possible cause of associative prosopagnosia might be the occurrence of Dynamic attractors in the brain's auto-associative circuits. We present a biologically plausible model composed of two stages: Pre-processing and face recognition. In the first stage, the face image is passed through Gabor filters which model the kind of visual processing carried out by the simple and complex cells of the primary visual cortex of higher mammals and the resulting features are fed into a Pseudo-inverse associative neural network for the recognition task. Next, we damage the network by reducing self-connections below a certain threshold in order to create dynamic attractors and hence hinder the networks ability to recognize familiar faces (faces already learned). Results obtained from simulations show that the resulting network responses are very similar to those of associative prosopagnosic patients. We conclude that the problems concerning associative prosopagnosia may partly be explained through the concepts of dynamic attractors. Although there is no known cure for prosopagnosia, we believe that the focus of any treatment should be to help the individual with prosopagnosia develop compensatory strategies for remembering faces. Adults with prosopagnosia as a result of stroke or brain trauma can be retrained to use other clues to identify faces. And a cure for children born with prosopagnosia might eventually rely on reinforcement techniques that reward them for paying attention to faces during early childhood. Reinforcement learning from examples of patterns to be classified using habituation and association would create lower dimensional local basins in the brain, which would form a global attractor landscape with one basin for each face. These local basins would eventually constitute dynamical memories that solve difficult problems in classifying and recognizing faces.     

On having royal relatives: Interpreting misidentifications in a case of impaired person recognition

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.