Perspectives on prosopagnosia and models of face recognition

The two papers by Bobes et al. (2003, this issue) and by Sperber and Spinnler (2003, this issue) add to the large body of literature demonstrating covert face recognition in prosopagnosia. This viewpoint will offer some perspectives on this interesting phenomenon. First, a re-analysis of the empirical literature will indicate an important misconception concerning the preserved abilities of prosopagnosics. The second section will briefly assess the contribution of Bobes et al. (2003, this issue) and Sperber and Spinnler (2003, this issue) to the debate about the locus, in cognitive terms, of the underlying causal deficit in prosopagnosia with covert face recognition. Both papers make reference to the two main models seeking to explain this phenomenon: the model proposed by Burton and colleagues (Burton et al., 1991; Burton and Young, 1999; Young and Burton, 1999) and that proposed by Farah and colleagues (Farah et al., 1993; O'Reilly and Farah, 1999). Finally, an observation will be offered concerning representations of faces in the Burton et al. (1991) model.     

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.     

Covert person recognition: its fadeout in a case of temporal lobe degeneration

Covert person recognition was investigated longitudinally over a three-year period in a patient suffering from "Crossmodal Familiar Person Agnosia", possibly due to a fronto-temporal dementia in its right temporal variant (Gentileschi et al., 2001). The progressive neuronal degeneration in the cortical regions critical for face recognition (viz., right infero-temporal areas) presented us with the opportunity to check Burton et al.'s (1991) and Farah et al.'s (1993) hypothesis on the dissociation between overt and covert face recognition in a neuropsychological condition which, however, is neurologically and cognitively different from that of focal "associative prosopagnosia". Covert person recognition starting from overtly unrecognised faces was assessed by means of learning tasks of face/name association involving celebrities. It was assumed that some unconsciously spared information would selectively enhance the relearning rates when famous faces were paired with their true names. In fact, the true-name advantage (i.e., selective saving for experimental relearning of true name pairings) reached significance at first assessment, carried out five years from clinical onset. Effect faded away two and three years later on, thus abolishing the overt/covert dissociation in face recognition. These findings support Burton et al.'s (1991) and Farah et al.'s (1993) hypothesis of covert face recognition as the consequence of partial and incomplete activation of person semantics, due, in the present case, to the impoverishment of Gentileschi et al.'s (2001) "exemplar semantics" storehouse. Moreover, it turned out that covert recognition does not imply a different learning slope, but an overall different level of the learning profile.     

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.     

Dissociations of face and object recognition in developmental prosopagnosia

Neuropsychological studies with patients suffering from prosopagnosia have provided the main evidence for the hypothesis that the recognition of faces and objects rely on distinct mechanisms. Yet doubts remain, and it has been argued that no case demonstrating an unequivocal dissociation between face and object recognition exists due in part to the lack of appropriate response time measurements (Gauthier et al., 1999). We tested seven developmental prosopagnosics to measure their accuracy and reaction times with multiple tests of face recognition and compared this with a larger battery of object recognition tests. For our systematic comparison, we used an old/new recognition memory paradigm involving memory tests for cars, tools, guns, horses, natural scenes, and houses in addition to two separate tests for faces. Developmental prosopagnosic subjects performed very poorly with the face memory tests as expected. Four of the seven prosopagnosics showed a very strong dissociation between the face and object tests. Systematic comparison of reaction time measurements for all tests indicates that the dissociations cannot be accounted for by differences in reaction times. Contrary to an account based on speed accuracy tradeoffs, prosopagnosics were systematically faster in nonface tests than in face tests. Thus, our findings demonstrate that face and nonface recognition can dissociate over a wide range of testing conditions. This is further support for the hypothesis that face and nonface recognition relies on separate mechanisms and that developmental prosopagnosia constitutes a disorder separate from developmental agnosia.     

Covert recognition in acquired and developmental prosopagnosia

BACKGROUND: Some patients with prosopagnosia have covert recognition, meaning that they retain some familiarity or knowledge of facial identity of which they are not aware. OBJECTIVE:To test the hypothesis that prosopagnosic patients with right occipitotemporal lesions and impaired face perception lack covert processing, whereas patients with associative prosopagnosia and bilateral anterior temporal lesions possess it. METHODS: Eight patients with prosopagnosia were tested with a battery of four face recognition tests to determine their ability to discriminate between famous and unknown faces. RESULTS: Measures of overt familiarity revealed better residual discrimination in patients with acquired prosopagnosia than in those with the developmental form. With forced-choice methods using famous faces paired with unknown faces, no patient demonstrated covert familiarity. However, when the semantic cue of the name of the famous face was provided, covert processing was present in all five patients with acquired prosopagnosia, including the three with extensive right-sided lesions and impaired perceptual discrimination of facial configuration. Sorting unrecognized faces by occupation was also performed above chance in three of these five patients. In contrast, none of the three patients with developmental prosopagnosia had covert processing, even though two demonstrated flawless performance on similar tests of name (rather than face) recognition. Overt familiarity correlated highly with the degree of covert recognition. CONCLUSIONS: Extensive right occipitotemporal lesions with significant deficits in face perception are not incompatible with covert face processing. Covert processing is absent in developmental prosopagnosia, because this condition likely precludes the establishment of a store of accurate facial memories. The presence of covert processing correlates with the degree of residual overt familiarity, indicating that these are related phenomena.     

Normal and abnormal face selectivity of the M170 response in developmental prosopagnosics

Developmental prosopagnosia is a lifelong impairment in face recognition despite normal low-level visual processing. Here we used magnetoencephalography (MEG) to examine the M170 response, a component occurring approximately 170 ms after stimulus onset, in a group of five developmental prosopagnosics. In normal subjects, the M170 is “face-selective”, with a consistently higher amplitude to faces than to a wide variety of other visual stimulus categories; the N170, a component recorded using event-related potentials (ERP) and thought to be analogous to the M170, also shows this “face selectivity”. Two previous ERP studies with developmental prosopagnosics have found attenuation or absence of face selectivity in the N170 response of these subjects [Bentin, S., Deouell, L. Y., & Soroker, N. (1999). Selective visual streaming in face recognition: Evidence from developmental prosopagnosia. Neuroreport, 10, 823–827; Kress, T., & Daum, I. (2003). Event-related potentials reflect impaired face recognition in patients with congenital prosopagnosia. Neuroscience Letters, 352, 133–136]. Three of our developmental prosopagnosic group showed this non-selective pattern at the M170 while the remaining two prosopagnosics were indistinguishable from normal controls. Thus, impaired face recognition is not necessarily correlated with an absence of the “face-selective” M170. Furthermore, ERP recordings collected simultaneously in the two developmental prosopagnosics with seemingly selective M170s also showed N170s within the same normal selective range, demonstrating that the face-selective signals found with MEG are not due to differences between MEG and ERP. While the presence of face selectivity at these neurophysiological markers is insufficient for predicting normal behavioral performance with faces, it could help to distinguish different classes of face recognition deficits.     

Covert face recognition in congenital prosopagnosia: a group study

IntroductionEven though people with congenital prosopagnosia (CP) never develop a normal ability to “overtly” recognize faces, some individuals show indices of “covert” (or implicit) face recognition. The aim of this study was to demonstrate covert face recognition in CP when participants could not overtly recognize the faces.MethodsEleven people with CP completed three tasks assessing their overt face recognition ability, and three tasks assessing their “covert” face recognition: a Forced choice familiarity task, a Forced choice cued task, and a Priming task.ResultsEvidence of covert recognition was observed with the Forced choice familiarity task, but not the Priming task. In addition, we propose that the Forced choice cued task does not measure covert processing as such, but instead “provoked-overt” recognition.ConclusionsOur study clearly shows that people with CP demonstrate covert recognition for faces that they cannot overtly recognize, and that behavioural tasks vary in their sensitivity to detect covert recognition in CP.     

Face and object imagery in congenital prosopagnosia: A case series

It has been reported that congenital prosopagnosics may have a general imagery deficit or an imagery deficit specific to faces. However, much of this evidence is based on self-report questionnaires, rather than experimentally based testing ( [Grüter et?al., 2007] and [Grüter et?al., 2009]). This study tested face and non-face based imagery in a case series of congenital prosopagnosics, utilising both questionnaire based and forced choice accuracy measures. Our findings indicate that all the prosopagnosics showed impaired face based imagery, which contrasted with normal performance on imagery of objects and colours - a pattern that is consistent with reports of acquired prosopagnosia ( [Barton, 2008] and [Michelon and Biederman, 2003]). Given all our experimentally based testing indicated face imagery impairments, despite no such problems being seen on self-report questionnaires, we would argue that testing based only on the latter must be interpreted with some caution. Overall, we would advocate that our findings demonstrate a category specific visual imagery impairment in congenital prosopagnosia, such that general imagery skill can be intact in such cases.     

Selective visual streaming in face recognition: evidence from developmental prosopagnosia

Computational considerations suggest that efficient face identification requires the categorization and exclusive streaming of previously encoded face visual primitives into a dedicated face recognition system. Unique evidence supporting this claim is provided by a rare case of developmental pure prosopagnosia with otherwise normal visual and cognitive functions. Despite his normal visual memory and ability to describe faces, he is extremely impaired in face recognition. An early event related brain potential (N170) that is normally elicited exclusively by human faces, showed no specificity in this person. MRI revealed a smaller then normal right temporal lobe. These data emphasize the indispensability of the early streaming process for face recognition.     

A new selective developmental deficit: Impaired object recognition with normal face recognition

Introduction

Studies of developmental deficits in face recognition, or developmental prosopagnosia, have shown that individuals who have not suffered brain damage can show face recognition impairments coupled with normal object recognition ( [Duchaine and Nakayama, 2005] , [Duchaine et?al., 2006] and [Nunn et?al., 2001] ). However, no developmental cases with the opposite dissociation – normal face recognition with impaired object recognition – have been reported. The existence of a case of non-face developmental visual agnosia would indicate that the development of normal face recognition mechanisms does not rely on the development of normal object recognition mechanisms.

Methods

To see whether a developmental variant of non-face visual object agnosia exists, we conducted a series of web-based object and face recognition tests to screen for individuals showing object recognition memory impairments but not face recognition impairments. Through this screening process, we identified AW, an otherwise normal 19-year-old female, who was then tested in the lab on face and object recognition tests.

Results

AW’s performance was impaired in within-class visual recognition memory across six different visual categories (guns, horses, scenes, tools, doors, and cars). In contrast, she scored normally on seven tests of face recognition, tests of memory for two other object categories (houses and glasses), and tests of recall memory for visual shapes. Testing confirmed that her impairment was not related to a general deficit in lower-level perception, object perception, basic-level recognition, or memory.

Discussion

AW’s results provide the first neuropsychological evidence that recognition memory for non-face visual object categories can be selectively impaired in individuals without brain damage or other memory impairment. These results indicate that the development of recognition memory for faces does not depend on intact object recognition memory and provide further evidence for category-specific dissociations in visual recognition.     

Dissociation between face perception and face memory in adults,but not children,with developmental prosopagnosia

Cognitive models propose that face recognition is accomplished through a series of discrete stages, including perceptual representation of facial structure, and encoding and retrieval of facial information. This implies that impaired face recognition can result from failures of face perception, face memory, or both. Studies of acquired prosopagnosia, autism spectrum disorders, and the development of normal face recognition support the idea that face perception and face memory are distinct processes, yet this distinction has received little attention in developmental prosopagnosia (DP). To address this issue, we tested the face perception and face memory of children and adults with DP. By definition, face memory is impaired in DP, so memory deficits were present in all participants. However, we found that all children, but only half of the adults had impaired face perception. Thus, results from adults indicate that face perception and face memory are dissociable, while the results from children provide no evidence for this division. Importantly, our findings raise the possibility that DP is qualitatively different in childhood versus adulthood. We discuss theoretical explanations for this developmental pattern and conclude that longitudinal studies are necessary to better understand the developmental trajectory of face perception and face memory deficits in DP.     

Behavioural and physiological evidence for covert face recognition in a prosopagnosic patient.

In a previous report, Bauer (1984) described the patient LF, who was unable to recognise familiar faces. Despite the inability to verbally identify familiar faces, psychophysiological examination revealed preserved covert processing of facial identity. Subsequent studies have demonstrated covert face recognition using behavioural tasks. Investigations of the patient PH showed normal face familiarity effects on matching, interference, priming, and learning tasks, while overt recognition was completely absent (De Haan, Young and Newcombe, 1987b). The use of different methodologies has led to different theoretical conceptualisation of the "covert recognition" phenomenon. Until now, no individual patient has been exposed to both methodologies. In this study we evaluated LF, who shows psychophysiological evidence of covert recognition, using behavioural tasks previously used with PH. The results reveal clear behavioural evidence of preserved face recognition without awareness. These findings suggest that both methodologies tap similar phenomena, and have important implications for theoretical models of covert face recognition. A conceptual model designed to integrate psychophysiological and behavioural evidence of covert face recognition is proposed.     

Covert face priming reveals a ‘true face effect’ in a case of congenital prosopagnosia

Previous research indicates that individuals with congenital prosopagnosia (CP) fail to demonstrate significant priming from faces to related names in covert recognition tasks. The interpretation has been that CP precludes the ability to acquire face representations. In the current study we replicated this important finding. In addition, we also demonstrated significant ‘true face effect’ in a CP patient, where face primes that matched the probe names facilitated reaction times compared to unrelated face primes. These data suggest that some individuals with CP may possess degraded face representations that facilitate the priming of a person's identity, but not semantic associates.     

Disorders of face perception and recognition

Face recognition is one of the most complex visual tasks performed by the human brain. Data from monkeys suggest that area IT may play a key role in identifying faces, and functional imaging research suggests that the human homologue of IT may be located in the medial occipitotemporal cortex, where a FFA has been located. Damage to medial occipitotemporal structures on the right or bilaterally leads to prosopagnosia, the failure to recognize facial identity. Prosopagnosia is not a single functional disorder but a family of dysfunctions, with different patients having different degrees of impairments to various perceptual and memory stages involved in face processing. Understanding the perceptual basis of this disorder and epiphenomena, such as covert recognition, is a goal of current research. Deficits in face perception also may contribute to Capgras syndrome and may be related to the impaired social development of patients with Asperger syndrome. More recently, identified deficits in face processing include the false recognition of unfamiliar faces and the impaired extraction of social information from faces, independent of the recognition of identity. Many of these prosopagnosia and other face processing deficits can be placed in the context of cognitive models of face processing stages, which are being refined continually by data from neurologic patients and functional imaging in normal subjects.     

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 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.     

Neurological disease and facial recognition

To discuss the neurological basis of facial recognition, we present our case reports of impaired recognition and a review of previous literature. First, we present a case of infarction and discuss prosopagnosia, which has had a large impact on face recognition research. From a study of patient symptoms, we assume that prosopagnosia may be caused by unilateral right occipitotemporal lesion and right cerebral dominance of facial recognition. Further, circumscribed lesion and degenerative disease may also cause progressive prosopagnosia. Apperceptive prosopagnosia is observed in patients with posterior cortical atrophy (PCA), pathologically considered as Alzheimer's disease, and associative prosopagnosia in frontotemporal lobar degeneration (FTLD). Second, we discuss face recognition as part of communication. Patients with Parkinson disease show social cognitive impairments, such as difficulty in facial expression recognition and deficits in theory of mind as detected by the reading the mind in the eyes test. Pathological and functional imaging studies indicate that social cognitive impairment in Parkinson disease is possibly related to damages in the amygdalae and surrounding limbic system. The social cognitive deficits can be observed in the early stages of Parkinson disease, and even in the prodromal stage, for example, patients with rapid eye movement (REM) sleep behavior disorder (RBD) show impairment in facial expression recognition. Further, patients with myotonic dystrophy type 1 (DM 1), which is a multisystem disease that mainly affects the muscles, show social cognitive impairment similar to that of Parkinson disease. Our previous study showed that facial expression recognition impairment of DM 1 patients is associated with lesion in the amygdalae and insulae. Our study results indicate that behaviors and personality traits in DM 1 patients, which are revealed by social cognitive impairment, are attributable to dysfunction of the limbic system.     

Searching for face-specific long latency ERPs: a topographic study of effects associated with mismatching features

In a previous study [E. Olivares, M.A. Bobes, E. Aubert, M. Valdés-Sosa, Associative ERPs effects with memories of artificial faces, Cogn. Brain Res. 2 (1994) 39–48] we reported the presence of a negativity associated with mismatching features when subjects carried out a face-feature matching task whilst their evoked potentials were recorded. Since the stimuli used were learned faces (realistic drawings), for which the subjects possessed no semantic information or associated verbal labels, the mismatch negativity obtained was considered a face-specific N400. In this work we present a new experiment to study the topographic distribution of these mismatch effects. As in the above-mentioned study, in each trial the subjects observed previously an incomplete (without the eyes/eyebrows fragment) familiar face, which served as a structural context for the face recognition. The face was then completed by grafting either matching (learned) features or mismatching features (from another face). In line with neuropsychological studies on prosopagnosia and electrophysiological findings in humans and non-human primates, we found as one of the most relevant items of data that the most-posterior (principally, left occipital) cortices appear to be a region in which are located the possible neural generators of the negativity associated with the detection of incongruencies in the structure of familiar faces. We also reported a late positivity, distributed in more anterior regions, which follows the mismatch negativity. This complex N–P is interpreted as reflecting a dual process of retrieval and integration of information in memory.