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.     

Whole not hole: Expert face recognition requires holistic perception

Face recognition is an important ability of the human brain, yet its underlying mechanisms are still poorly understood. Two opposite views have been proposed to account for human face recognition expertise: the ability to extract the most diagnostic local information, feature-by feature (analytical view), or the ability to process all features at once over the whole face (holistic view). To help clarifying this debate, we used an original gaze-contingent stimulus presentation method to compare normal observers and a brain-damaged patient specifically impaired at face recognition (prosopagnosia). When a single central facial feature was revealed at a time through a gaze-contingent window, normal observers’ performance at an individual face matching task decreased to the patient level. However, when only the central feature was masked, forcing normal observers to rely on the whole face but the fixated feature, their performance was almost not affected. In contrast, the prosopagnosic patient's performance decreased dramatically in this latter condition. These results were independent of the absolute size of the face and window/mask. This dissociation indicates that expertise in face recognition does not rest on the ability to analyze diagnostic local detailed features sequentially but rather on the ability to see the individual features of a face all at once, a function that is critically impaired in acquired prosopagnosia.     

Impairment of holistic face perception following right occipito-temporal damage in prosopagnosia: converging evidence from gaze-contingency

Gaze-contingency is a method traditionally used to investigate the perceptual span in reading by selectively revealing/masking a portion of the visual field in real time. Introducing this approach in face perception research showed that the performance pattern of a brain-damaged patient with acquired prosopagnosia (PS) in a face matching task was reversed, as compared to normal observers: the patient showed almost no further decrease of performance when only one facial part (eye, mouth, nose, etc.) was available at a time (foveal window condition, forcing part-based analysis), but a very large impairment when the fixated part was selectively masked (mask condition, promoting holistic perception) ( [Van Belle et al., 2010a] and [Van Belle et al., 2010b] ). Here we tested the same manipulation in a recently reported case of pure prosopagnosia (GG) with unilateral right hemisphere damage (Busigny, Joubert, Felician, Ceccaldi, & Rossion, 2010). Contrary to normal observers, GG was also significantly more impaired with a mask than with a window, demonstrating impairment with holistic face perception. Together with our previous study, these observations support a generalized account of acquired prosopagnosia as a critical impairment of holistic (individual) face perception, implying that this function is a key element of normal human face recognition. Furthermore, the similar behavioral pattern of the two patients despite different lesion localizations supports a distributed network view of the neural face processing structures, suggesting that the key function of human face processing, namely holistic perception of individual faces, requires the activity of several brain areas of the right hemisphere and their mutual connectivity.     

Impaired holistic coding of facial expression and facial identity in congenital prosopagnosia

We test 12 individuals with congenital prosopagnosia (CP), who replicate a common pattern of showing severe difficulty in recognising facial identity in conjunction with normal recognition of facial expressions (both basic and ‘social’). Strength of holistic processing was examined using standard expression composite and identity composite tasks. Compared to age- and sex-matched controls, group analyses demonstrated that CPs showed weaker holistic processing, for both expression and identity information. Implications are (a) normal expression recognition in CP can derive from compensatory strategies (e.g., over-reliance on non-holistic cues to expression); (b) the split between processing of expression and identity information may take place after a common stage of holistic processing; and (c) contrary to a recent claim, holistic processing of identity is functionally involved in face identification ability.     

Impaired processing of relative distances between features and of the eye region in acquired prosopagnosia—Two sides of the same holistic coin?

Acquired prosopagnosia (AP) is characterized by impaired recognition of individual faces following brain damage. The nature of the functional impairment(s) underlying AP remains debated. Recent studies have demonstrated deficient processing of diagnostic information in the region of the eyes (Caldara et al., 2005); other studies suggest that patients fail to judge relative distances between facial features (Barton et al., 2002). We hypothesized that these apparently different observations are related to a common cause. More precisely, we suggest that AP arises due to an impairment of a process that reduces uncertainty about the nature/location of the diagnostic cues for face individualization: the ability to perceive multiple elements of a face as a single global representation (holistic processing). Being impaired at processing individual faces holistically, prosopagnosic patients would tend to perform relatively worse for processing facial areas containing multiple elements (i.e., the eyes), and for elements that are widely spaced apart. Here we tested PS, a single case of AP, at matching unfamiliar faces differing either with respect to local features or inter-feature distances, over the upper and lower areas of the face. A pilot study and Experiment 1 confirmed that PS was extremely poor at using information encompassing the eyes, but was also deficient at perceiving relative distances between features. When uncertainty about the location and nature of the diagnostic cue was removed in Experiment 2, PS' performance remained below normal range, but she improved substantially. Most interestingly, her pattern of performance across the different conditions appeared qualitatively identical to that of normal controls. In line with previous observations of PS and other cases of prosopagnosia, our findings indicate that the reduced reliance on the area of the eyes and on relative distances between features in AP may have a common underlying cause—the disruption of holistic processing of the individual face.     

Acquired prosopagnosia abolishes the face inversion effect

Individual faces are notoriously difficult to recognize when they are presented upside-down. Since acquired prosopagnosia (AP) has been associated with an impairment of expert face processes, a reduced or abolished face inversion effect (FIE) is expected in AP. However, previous studies have incongruently reported apparent normal effects of inversion, a decreased or abolished FIE, but also a surprisingly better performance for inverted faces for some patients. While these discrepant observations may be due to the variability of high-level processes impaired, a careful look at the literature rather suggests that the pattern of FIE in prosopagnosia has been obscured by a selection of patients with associated low-level defects and general visual recognition impairments, as well as trade-offs between accuracy and correct RT measures. Here we conducted an extensive investigation of upright and inverted face processing in a well-characterized case of face-selective AP, PS (Rossion et al., 2003). In 4 individual face discrimination experiments, PS did not present any inversion effect at all, taking into account all dependent measures of performance. However, she showed a small inversion cost for individualizing members of a category of non-face objects (cars), just like normal observers. A fifth experiment with personally familiar faces to recognize confirmed the lack of inversion effect for PS. Following the present report and a survey of the literature, we conclude that the FIE is generally absent, or at least clearly reduced following AP. We also suggest that the paradoxical superior performance for inverted faces observed in rare cases may be due to additional upper visual field defects rather than to high-level competing visual processes. These observations are entirely compatible with the view that AP is associated with a disruption of a process that is also abolished following inversion: the holistic representation of individual exemplars of the face class.     

Emotional attention in acquired prosopagnosia

The present study investigated whether emotionally expressive faces guide attention and modulate fMRI activity in fusiform gyrus in acquired prosopagnosia. Patient PS, a pure case of acquired prosopagnosia with intact right middle fusiform gyrus, performed two behavioral experiments and a functional imaging experiment to address these questions. In a visual search task involving face stimuli, PS was faster to select the target face when it was expressing fear or happiness as compared to when it was emotionally neutral. In a change detection task, PS detected significantly more changes when the changed face was fearful as compared to when it was neutral. Finally, an fMRI experiment showed enhanced activation to emotionally expressive faces and bodies in right fusiform gyrus. In addition, PS showed normal body-selective activation in right fusiform gyrus, partially overlapping the fusiform face area. Together these behavioral and neuroimaging results show that attention was preferentially allocated to emotional faces in patient PS, as observed in healthy subjects. We conclude that systems involved in the emotional guidance of attention by facial expression can function normally in acquired prosopagnosia, and can thus be dissociated from systems involved in face identification.     

The anatomic basis of the right face-selective N170 IN acquired prosopagnosia: a combined ERP/fMRI study

The N170 waveform is larger over posterior temporal cortex when healthy subjects view faces than when they view other objects. Source analyses have produced mixed results regarding whether this effect originates in the fusiform face area (FFA), lateral occipital cortex, or superior temporal sulcus (STS), components of the core face network. In a complementary approach, we assessed the face-selectivity of the right N170 in five patients with acquired prosopagnosia, who also underwent structural and functional magnetic resonance imaging. We used a non-parametric bootstrap procedure to perform single-subject analyses, which reliably confirmed N170 face-selectivity in each of 10 control subjects. Anterior temporal lesions that spared the core face network did not affect the face-selectivity of the N170. A face-selective N170 was also present in another subject who had lost only the right FFA. However, face-selectivity was absent in two patients with lesions that eliminated the occipital face area (OFA) and FFA, sparing only the STS. Thus while the right FFA is not necessary for the face-selectivity of the N170, neither is the STS sufficient. We conclude that the face-selective N170 in prosopagnosia requires residual function of at least two components of the core face-processing network.     

Covert matching of unfamiliar faces in a case of prosopagnosia: an ERP study

In addition to their deficit in overt face recognition, patients with prosopagnosia also have difficulties in matching sequentially presented unfamiliar faces. Here we assessed the possibility that covert matching of faces was present in a case with prosopagnosia using event-related potentials (ERPs). The participants (patient FE and normal controls) were challenged with a face-identity matching task, in which they decided whether two sequentially presented photographs of unfamiliar faces represented the same person. Only internal face features were used and the two faces in a pair differed in emotional expression. FE failed to overtly match these stimuli. In contrast, the ERPs revealed evidence of covert matching. If the two faces within a pair of stimuli depicted different posers, then the response to the second face contained an enhanced N300 compared to the situation where the identity of the faces was the same. The latency of the N300 was the same as a similar component found in controls. These results suggest that some cases with prosopagnosia have a covert ability to match unfamiliar faces, with similar temporal dynamics as controls, which in contrast with the idea that a generalized slowing of face processing occurs in all cases of prosopagnosia.     

Event-related potentials reflect heterogeneity of developmental prosopagnosia

Event-related potential (ERP) studies of developmental prosopagnosia (DP) are rare. Previous ERP investigations have reported smaller N170 amplitude differences between faces and objects in at least three prosopagnosics. The present study is based on a combination of behavioural and electrophysiological assessment of face processing. The aim was to investigate the face-specificity of the N170 in both healthy subjects and a group of DP individuals (N = 4), using famous and nonfamous faces, caricatures and houses as stimuli. All prosopagnosic subjects showed impairments in recognition of famous faces, memory for faces and learning new faces in behavioural assessment. In healthy subjects the largest effects were found at parieto-occipital electrode positions (PO7 and PO8), along with a familiarity effect at these electrode positions. Thus, parieto-occipital areas appear to play an important role in face processing. Three prosopagnosics showed reliable N170 amplitude differences between faces and nonface stimuli, whereas one DP individual showed significantly reduced amplitude differences between faces and nonface objects. The behavioural and electrophysiological data support the idea that DP reflects a heterogeneous impairment and that face processing deficits are not necessarily correlated with a lack of face-specific N170.     

Right perceptual bias and self-face recognition in individuals with congenital prosopagnosia

The existence of a drift to base judgments more on the right half-part of facial stimuli, which falls in the observer's left visual field (left perceptual bias (LPB)), in normal individuals has been demonstrated. However, less is known about the existence of this phenomenon in people affected by face impairment from birth, namely congenital prosopagnosics. In the current study, we aimed to investigate the presence of the LPB under face impairment conditions using chimeric stimuli and the most familiar face of all: the self-face. For this purpose we tested 10 participants with congenital prosopagnosia and 21 healthy controls with a face matching task using facial stimuli, involving a spatial manipulation of the left and the right hemi-faces of self-photos and photos of others. Even though congenital prosopagnosics performance was significantly lower than that of controls, both groups showed a consistent self-face advantage. Moreover, congenital prosopagnosics showed optimal performance when the right side of their face was presented, that is, right perceptual bias, suggesting a differential strategy for self-recognition in those subjects. A possible explanation for this result is discussed.     

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.     

Evidence of an eye movement-based memory effect in congenital prosopagnosia

While extensive work has examined the role of covert recognition in acquired prosopagnosia, little attention has been directed to this process in the congenital form of the disorder. Indeed, evidence of covert recognition has only been demonstrated in one congenital case in which autonomic measures provided evidence of recognition (Jones and Tranel, 2001), whereas two investigations using behavioural indicators failed to demonstrate the effect (de Haan and Campbell, 1991; Bentin et al., 1999). In this paper, we use a behavioural indicator, an "eye movement-based memory effect" (Althoff and Cohen, 1999), to provide evidence of covert recognition in congenital prosopagnosia. In an initial experiment, we examined viewing strategies elicited to famous and novel faces in control participants, and found fewer fixations and reduced regional sampling for famous compared to novel faces. In a second experiment, we examined the same processes in a patient with congenital prosopagnosia (AA), and found some evidence of an eye movement-based memory effect regardless of his recognition accuracy. Finally, we examined whether a difference in scanning strategy was evident for those famous faces AA failed to explicitly recognise, and again found evidence of reduced sampling for famous faces. We use these findings to (a) provide evidence of intact structural representations in a case of congenital prosopagnosia, and (b) to suggest that covert recognition can be demonstrated using behavioural indicators in this disorder.     

A computational model of dysfunctional facial encoding in congenital prosopagnosia

Congenital prosopagnosia is a selective deficit in face identification that is present from birth. Previously, behavioral deficits in face recognition and differences in the neuroanatomical structure and functional activation of face processing areas have been documented mostly in separate studies. Here, we propose a neural network model of congenital prosopagnosia which relates behavioral and neuropsychological studies of prosopagnosia to theoretical models of information processing.In this study we trained a neural network with two different algorithms to represent face images. First, we introduced a predisposition towards a decreased network connectivity implemented as a temporal independent component analysis (ICA). This predisposition induced a featural representation of faces in terms of isolated face parts. Second, we trained the network for optimal information encoding using spatial ICA, which led to holistic representations of faces. The network model was then tested empirically in an experiment with ten prosopagnosic and twenty age-matched controls. Participants had to discriminate between faces that were changed either according to the prosopagnosic model of featural representation or to the control model of holistic representation. Compared to controls prosopagnosic participants were impaired only in discriminating holistic changes of faces but showed no impairment in detecting featural changes.In summary, the proposed model presents an empirically testable account of congenital prosopagnosia that links the critical features — a lack of holistic processing at the computational level and a sparse structural connectivity at the implementation level. More generally, our results point to structural differences in the network connectivity as the cause of the face processing deficit in congenital prosopagnosia.     

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.     

Electrophysiological correlates of processing faces of younger and older individuals

The 'own-age bias' in face processing suggests that the age of a face constitutes one important factor that influences attention to and memory for faces. The present experiment investigated electrophysiological correlates of processing faces of younger and older individuals. Younger participants were presented with pictures of unfamiliar younger and older faces in the context of a gender categorization task. A comparison of event-related potentials showed that early components are sensitive to faces of different ages: (i) larger positive potential peaking at 160 ms (P200) for older than younger faces at fronto-central electrodes; (ii) larger negative potential peaking at 252 ms (N200) for younger than older faces at fronto-central electrodes; (iii) larger negative-going deflection peaking at 320 ms (N250) for younger than older faces at occipito-temporal electrodes; and (iv) larger late positive potential peaking at 420 ms (LPP 420) for older than younger faces at parietal and other electrodes. We discuss similarities between the present study and a previously published study of faces of different races as suggesting involvement of comparable electrophysiological responses when differentiating between stimulus categories.     

Influences of spontaneous perspective taking on spatial and identity processing of faces

Previous research suggests that people, when interacting with another agent, are sensitive to the other’s visual perspective on the scene. The present study investigated how spontaneously another’s different spatial perspective is taken into account and how this affects the processing of jointly attended stimuli. Participants viewed upright or inverted faces alone, next to another person (same spatial perspective), or opposite another person (different spatial perspectives) while electroencephalography (EEG) was recorded. The task (counting male faces) was in no way related to spatial aspects of the stimuli, and thus did not encourage perspective taking. EEG results revealed no general differences between viewing faces alone or with another person. However, when holding different perspectives (sitting opposite each other), the amplitudes of the N170 and of the N250 significantly increased for upright faces. This indicates that people spontaneously represented the other’s different perspective, which led to higher demands for structural encoding (N170) and to increased allocation of attention to face recognition (N250) for stimuli that are typically processed configurally. When holding different spatial perspectives, thus, people may not merely represent that the other sees the object or scene differently, but how the object/scene looks for the other.     

Inverted face processing in body dysmorphic disorder

Individuals with body dysmorphic disorder (BDD) are preoccupied with perceived defects in appearance. Preliminary evidence suggests abnormalities in global and local visual information processing. The objective of this study was to compare global and local processing in BDD subjects and healthy controls by testing the face inversion effect, in which inverted (upside-down) faces are recognized more slowly and less accurately relative to upright faces. Eighteen medication-free subjects with BDD and 17 matched, healthy controls performed a recognition task with sets of upright and inverted faces on a computer screen that were either presented for short duration (500 ms) or long duration (5000 ms). Response time and accuracy rates were analyzed using linear and logistic mixed effects models, respectively. Results indicated that the inversion effect for response time was smaller in BDD subjects than controls during the long duration stimuli, but was not significantly different during the short duration stimuli. Inversion effect on accuracy rates did not differ significantly between groups during either of the two durations. Lesser inversion effect in BDD subjects may be due to greater detail-oriented and piecemeal processing for long duration stimuli. Similar results between groups for short duration stimuli suggest that they may be normally engaging configural and holistic processing for brief presentations. Abnormal visual information processing in BDD may contribute to distorted perception of appearance; this may not be limited to their own faces, but to others’ faces as well.     

Face recognition in schizophrenia disorder: A comprehensive review of behavioral,neuroimaging and neurophysiological studies

Facial emotion processing has been extensively studied in schizophrenia patients while general face processing has received less attention. The already published reviews do not address the current scientific literature in a complete manner. Therefore, here we tried to answer some questions that remain to be clarified, particularly: are the non-emotional aspects of facial processing in fact impaired in schizophrenia patients? At the behavioral level, our key conclusions are that visual perception deficit in schizophrenia patients: are not specific to faces; are most often present when the cognitive (e.g. attention) and perceptual demands of the tasks are important; and seems to worsen with the illness chronification. Although, currently evidence suggests impaired second order configural processing, more studies are necessary to determine whether or not holistic processing is impaired in schizophrenia patients. Neural and neurophysiological evidence suggests impaired earlier levels of visual processing, which might involve the deficits in interaction of the magnocellular and parvocellular pathways impacting on further processing. These deficits seem to be present even before the disorder out-set. Although evidence suggests that this deficit may be not specific to faces, further evidence on this question is necessary, in particularly more ecological studies including context and body processing.