Developmental prosopagnosia and super-recognition: no special role for surface reflectance processing

Face recognition by normal subjects depends in roughly equal proportions on shape and surface reflectance cues, while object recognition depends predominantly on shape cues. It is possible that developmental prosopagnosics are deficient not in their ability to recognize faces per se, but rather in their ability to use reflectance cues. Similarly, super-recognizers' exceptional ability with face recognition may be a result of superior surface reflectance perception and memory. We tested this possibility by administering tests of face perception and face recognition in which only shape or reflectance cues are available to developmental prosopagnosics, super-recognizers, and control subjects. Face recognition ability and the relative use of shape and pigmentation were unrelated in all the tests. Subjects who were better at using shape or reflectance cues were also better at using the other type of cue. These results do not support the proposal that variation in surface reflectance perception ability is the underlying cause of variation in face recognition ability. Instead, these findings support the idea that face recognition ability is related to neural circuits using representations that integrate shape and pigmentation information.     

Disconnection in prosopagnosia and face processing

Face perception is a function with significant complexity, reflected in cognitive models that propose a hierarchy of parallel and serial processing stages. Current neuroimaging data also show that face perception involves a core processing network of cortical modules, which are likely specialized for different functions involved in face processing. The core face processing network is further linked to an extended face processing network which is not solely involved in the perception of faces, but rather contains modules mediating the processing of semantic, biographic and emotional information about people. The segregation of these processes within discrete anatomic regions creates the potential for disconnection between regions to generate neuropsychological deficits involving faces. In this review we consider the types of disconnection possible both within the core face processing system and between the core and extended systems, the pattern of deficits that would be considered as evidence of such disconnections, the potential anatomy of lesions that would create them, and whether any cases exist that meet these criteria.     

Impaired holistic processing in congenital prosopagnosia

It has long been argued that face processing requires disproportionate reliance on holistic or configural processing, relative to that required for non-face object recognition, and that a disruption of such holistic processing may be causally implicated in prosopagnosia. Previously, we demonstrated that individuals with congenital prosopagnosia (CP) did not show the normal face inversion effect (better performance for upright compared to inverted faces) and evinced a local (rather than the normal global) bias in a compound letter global/local (GL) task, supporting the claim of disrupted holistic processing in prosopagnosia. Here, we investigate further the nature of holistic processing impairments in CP, first by confirming, in a large sample of CP individuals, the absence of the normal face inversion effect and the presence of the local bias on the GL task, and, second, by employing the composite face paradigm, often regarded as the gold standard for measuring holistic face processing. In this last task, we show that, in contrast with controls, the CP group perform equivalently with aligned and misaligned faces and was impervious to (the normal) interference from the task-irrelevant bottom part of faces. Interestingly, the extent of the local bias evident in the composite task is correlated with the abnormality of performance on diagnostic face processing tasks. Furthermore, there is a significant correlation between the magnitude of the local bias in the GL and performance on the composite task. These results provide further evidence for impaired holistic processing in CP and, moreover, corroborate the critical role of this type of processing for intact face recognition.     

Dysfunction in configural face processing in patients with schizophrenia

BACKGROUND: Face recognition has important implications for patients with schizophrenia, who exhibit poor interpersonal and social skills. Previous reports have suggested that patients with schizophrenia have deficits in their ability to recognize faces, and because face recognition relies heavily on information about the configuration of faces, we hypothesized that patients with schizophrenia would have specific problems in processing configural information. METHODS: We measured the performance of 20 patients with schizophrenia and 20 normal subjects in a face-discrimination task, using upright and inverted pairs of face photographs that differed in featural or configural information. RESULTS: The patients with schizophrenia showed disproportionately poorer performance in discriminating configural compared with featural face sets. CONCLUSION: The result suggests that the face-recognition deficit in schizophrenic patients is due to specific impairments in configural processing of faces.     

Developmental prosopagnosia and the Benton Facial Recognition Test

The Benton Facial Recognition Test is used for clinical and research purposes, but evidence suggests that it is possible to pass the test with impaired face discrimination abilities. The authors tested 11 patients with developmental prosopagnosia using this test, and a majority scored in the normal range. Consequently, scores in the normal range should be interpreted cautiously, and testing should always be supplemented by other face tests.     

Global and configural visual processing in adults with autism and Asperger syndrome

This study was designed to explore how adults with autism and Asperger syndrome (ASD) would visually process compound figures. They were tested in two tasks, one involving hierarchical global/local stimuli, the other involving face-like or geometrical stimuli where the processing of the inter-elemental spatial relationships was emphasized. Adults with ASD showed, like controls, a preference for the global level of the hierarchical stimuli. With the stimuli involving inter-elemental spatial relationship manipulations, the adults with ASD showed a preference for local elements, whereas controls did not show a preference. This supports earlier findings from children with ASD, suggesting that though individuals with autism may process global aspects of stimuli in priority, they tend to specific aspects in stimuli containing both local and configural elements.     

Event-related potentials show configural specificity of global form processing

Glass patterns are a type of moiré created when a random-dot field is overlaid with a rotated, translated or dilated copy. The overall form of the moiré cannot be detected using local processing mechanisms, and because of this, Glass patterns are useful probes of global form processing. Here, we use event-related potentials to show that certain global organizations (concentric structure created by rotation and radial structure produced by dilation) produce much larger brain responses than others (linear structure created by translation). The results are consistent with the existence of specialized form processing mechanisms in the extrastriate cortex.     

Developmental prosopagnosia with concurrent topographical difficulties: A case report and virtual reality training programme

Several neuropsychological case studies report brain-damaged individuals with concurrent impairments in face recognition (i.e., prosopagnosia) and topographical orientation. Recently, individuals with a developmental form of topographical disorientation have also been described, and several case reports of individuals with developmental prosopagnosia provide anecdotal evidence of concurrent navigational difficulties. Clearly, the co-occurrence of these difficulties can exacerbate the negative psychosocial consequences associated with each condition. This paper presents the first detailed case report of an individual (FN) with developmental prosopagnosia alongside difficulties in topographical orientation. FN’s performance on an extensive navigational battery indicated that she primarily has difficulties in the formation and retrieval of cognitive maps. We then evaluated the effectiveness of a short-term virtual reality training programme and found that she is able to form a cognitive map of a particular environment following intense overlearning. Surprisingly, FN’s performance on a face recognition task also improved following training. While the latter finding was unexpected and requires further exploration, the training programme reported here may help to alleviate some of the compounded negative psychosocial consequences that are associated with difficulties in finding both locations and people.     

Impaired holistic processing of unfamiliar individual faces in acquired prosopagnosia

Prosopagnosia is an impairment at individualizing faces that classically follows brain damage. Several studies have reported observations supporting an impairment of holistic/configural face processing in acquired prosopagnosia. However, this issue may require more compelling evidence as the cases reported were generally patients suffering from integrative visual agnosia, and the sensitivity of the paradigms used to measure holistic/configural face processing in normal individuals remains unclear. Here we tested a well-characterized case of acquired prosopagnosia (PS) with no object recognition impairment, in five behavioral experiments (whole/part and composite face paradigms with unfamiliar faces). In all experiments, for normal observers we found that processing of a given facial feature was affected by the location and identity of the other features in a whole face configuration. In contrast, the patient's results over these experiments indicate that she encodes local facial information independently of the other features embedded in the whole facial context. These observations and a survey of the literature indicate that abnormal holistic processing of the individual face may be a characteristic hallmark of prosopagnosia following brain damage, perhaps with various degrees of severity.     

Compensatory strategies in processing facial emotions: evidence from prosopagnosia

We report data on the processing of facial emotion in a prosopagnosic patient (H.J.A.). H.J.A. was relatively accurate at discriminating happy from angry upright faces, but he performed at chance when the faces were inverted. Furthermore, with upright faces there was no configural interference effect on emotion judgements, when face parts expressing different emotions were aligned to express a new emergent emotion. We propose that H.J.A.'s emotion judgements relied on local rather than on configural information, and this local information was disrupted by inversion. A compensatory strategy, based on processing local face parts, can be sufficient to process at least some facial emotions.     

Training with own-race faces can improve processing of other-race faces: evidence from developmental prosopagnosia

Faces of one's own race are discriminated and recognized more accurately than faces of an other race (other-race effect - ORE). Studies have employed several methods to enhance individuation and recognition of other-race faces and reduce the ORE, including intensive perceptual training with other-race faces and explicitly instructing participants to individuate other-race faces. Unfortunately, intensive perceptual training has shown to be specific to the race trained and the use of explicit individuation strategies, though applicable to all races, can be demanding of attention and difficult to consistently employ. It has not yet been demonstrated that a training procedure can foster the automatic individuation of all other-race faces, not just faces from the race trained. Anecdotal evidence from a training procedure used with developmental prosopagnosics (DPs) in our lab, individuals with lifelong face recognition impairments, suggests that this may be possible. To further test this idea, we had five Caucasian DPs perform ten days of configural face training (i.e. attending to small spacing differences between facial features) with own-race (Caucasian) faces to see if training would generalize to improvements with other-race (Korean) faces. To assess training effects and localize potential effects to parts-based or holistic processing, we used the part-whole task using Caucasian and Korean faces (Tanaka, J. W., Kiefer, M., & Bukach, C. M. (2004). A holistic account of the own-race effect in face recognition: evidence from a cross-cultural study. Cognition, 93(1), B1-9). Results demonstrated that after training, DPs showed a disproportionate improvement in holistic processing of other-race faces compared to own-race faces, reducing their ORE. This suggests that configural training with own-race faces boosted DPs’ general configural/holistic attentional resources, which they were able to apply to other-race faces. This provides a novel method to reduce the ORE and supports more of an attentional/social-cognitive model of the ORE rather than a strictly expertise model.     

Congenital prosopagnosia: multistage anatomical and functional deficits in face processing circuitry

Face recognition is a primary social skill which depends on a distributed neural network. A pronounced face recognition deficit in the absence of any lesion is seen in congenital prosopagnosia. This study investigating 24 congenital prosopagnosic subjects and 25 control subjects aims at elucidating its neural basis with fMRI and voxel-based morphometry. We found a comprehensive behavioral pattern, an impairment in visual recognition for faces and buildings that spared long-term memory for faces with negative valence. Anatomical analysis revealed diminished gray matter density in the bilateral lingual gyrus, the right middle temporal gyrus, and the dorsolateral prefrontal cortex. In most of these areas, gray matter density correlated with memory success. Decreased functional activation was found in the left fusiform gyrus, a crucial area for face processing, and in the dorsolateral prefrontal cortex, whereas activation of the medial prefrontal cortex was enhanced. Hence, our data lend strength to the hypothesis that congenital prosopagnosia is explained by network dysfunction and suggest that anatomic curtailing of visual processing in the lingual gyrus plays a substantial role. The dysfunctional circuitry further encompasses the fusiform gyrus and the dorsolateral prefrontal cortex, which may contribute to their difficulties in long-term memory for complex visual information. Despite their deficits in face identity recognition, processing of emotion related information is preserved and possibly mediated by the medial prefrontal cortex. Congenital prosopagnosia may, therefore, be a blueprint of differential curtailing in networks of visual cognition.     

Detailed exploration of face-related processing in congenital prosopagnosia: 1. Behavioral findings

We show that five individuals with congenital prosopagnosia (CP) are impaired at face recognition and discrimination and do not exhibit the normal superiority for upright over inverted faces despite intact visual acuity, low-level vision and intelligence, and in the absence of any obvious neural concomitant. Interestingly, the deficit is not limited to faces: The CP individuals were also impaired at discriminating common objects and novel objects although to a lesser extent than discriminating faces. The perceptual deficit may be attributable to a more fundamental visual processing disorder; the CP individuals exhibited difficulty in deriving global configurations from simple visual stimuli, even with extended exposure duration and considerable perceptual support in the image. Deriving a global configuration from local components is more critical for faces than for other objects, perhaps accounting for the exaggerated deficit in face processing. These findings elucidate the psychological mechanisms underlying CP and support the link between configural and face processing.     

Understanding memory for faces in Parkinson's disease: the role of configural processing

It has previously been reported that unfamiliar face recognition memory is impaired in Parkinson's disease (PD) [(Dewick, H. C., Hanley, J. R., Davies, A. D. M., Playfer, J. R. & Turnbull, C. J., Perception and memory for faces in Parkinson's disease. Neuropsychologia, 1991, 29, 785-802), (Haeske-Dewick, H. C., Are perception and memory for faces influenced by a specific age at onset factor in Parkinson's disease? Neuropsychologia, 1996, 34, 315-320), (Levin, B. E., Llabre, M. M. & Weiner, W. J., Cognitive impairments associated with early Parkinson's disease. Neurology, 1989, 39, 557-561)]. In the work reported here, we consider the possible mechanisms that might underlie this impairment. 28 PD patients and 28 controls were given a two-part test of recognition memory for words and faces, and two perceptual tests to measure their configural and componential processing ability. We found that PD patients were significantly worse than controls on the recognition memory test for faces, but not when the stimuli were words. In addition, PD patients were significantly impaired relative to controls on the closure test (FCT) used to measure configural processing, but there was no difference between the two groups on a test of componential processing ability. Multiple regression analyses revealed that even after accounting for the influence of age, intelligence and level of depression, configural processing ability was the important predictor of unfamiliar face recognition memory in Parkinson's disease. There was no effect of Parkinson's disease specific variables on either face recognition or FCT performance. In addition, some recently diagnosed patients were poor at face recognition. It is suggested that face configuration skills may be affected very early in the course of Parkinson's disease, and that this may be connected to the fact that considerable nigrostriatal degeneration and alteration in brain neurotransmitter levels occur before the clinical symptoms of PD appear.     

Featural versus configural face processing in a rare genetic disorder: Williams syndrome

Background Williams syndrome (WMS) is a rare genetic disorder with an estimated prevalence of 1 in 20 000 live births. Among other characteristics, WMS has a distinctive cognitive profile with spared face processing and language skills that contrasts with impairment in the cognitive domains of spatial cognition, problem solving and planning. It remains unclear whether individuals with WMS process faces using a featural strategy that focuses on features or a configural strategy that takes into consideration the contour of a face and spatial relations between features. Methods To investigate face processing in WMS, the tasks specifically probe unfamiliar face matching by using a design that includes manipulations in face presentation (thatcherised and non‐thatcherised), face orientation (upright and inverted) and face valence (happy and neutral expression) in a match‐to‐target face recognition design. The sample consisted of 20 participants with WMS, 10 participants with non‐specific developmental delay (IQ‐matched) and 10 normal control participants (chronological age‐matched). Results Similar to normal controls, WMS performed best when faces were presented upright. The results show while the WMS group did not perform as well as their typically developing counterparts, they did significantly better than the IQ‐matched developmentally delayed group. WMS did not show an accuracy advantage for inverted faces commonly understood as an index for featural face processing, nor did they perform better on thatcherised inverted face conditions whereby featural processing is forced. Furthermore, no accuracy advantage was observed for positively valenced (happy) faces in the WMS group. Conclusion These results are consistent with previous work showing a configural face processing approach in WMS, a strategy that is also utilised by normal controls.