Covert face recognition in prosopagnosia: A review

Prosopagnosia, a spectacular face agnosia, is generally detected and discussed on the basis of explicit or overt performance of the subjects. However, recent observations suggest that an overt response is probably not sufficient to determine what is and what is not preserved in the cognitive processing of faces by prosopagnosia. Indeed, signs of covert knowledge have been evidenced in some, but not all, subjects, indicating that they are still able to use representations they cannot use overtly. Empirical data, showing that the nature of prosopagnosia is a more complex phenomenon than has been thought and that the processing models should be adjusted accordingly, are reviewed.     

Neural and genetic foundations of face recognition and prosopagnosia

Faces are of essential importance for human social life. They provide valuable information about the identity, expression, gaze, health, and age of a person. Recent face‐processing models assume highly interconnected neural structures between different temporal, occipital, and frontal brain areas with several feedback loops. A selective deficit in the visual learning and recognition of faces is known as prosopagnosia, which can be found both in acquired and congenital form. Recently, a hereditary sub‐type of congenital prosopagnosia with a very high prevalence rate of 2.5% has been identified. Recent research results show that hereditary prosopagnosia is a clearly circumscribed face‐processing deficit with a characteristic set of clinical symptoms. Comparing face processing of people of prosopagnosia with that of controls can help to develop a more conclusive and integrated model of face processing. Here, we provide a summary of the current state of face processing research. We also describe the different types of prosopagnosia and present the set of typical symptoms found in the hereditary type. Finally, we will discuss the implications for future face recognition research.     

Understanding covert recognition

An implementation of Bruce and Young's (1986) functional model of face recognition is used to examine patterns of covert face recognition previously reported in a prosopagnosic patient, PH. Although PH is unable to recognize overly the faces of people known to him, he shows normal patterns of face processing when tested indirectly. A simple manipulation of one set of connections in the implemented model induces behaviour consistent with patterns of results from PH obtained in semantic priming and interference tasks. We compare this account with previous explanations of covert recognition and demonstrate that the implemented model provides the most natural and parsimonious account available. Two further patients are discussed who show deficits in person perception. The first (MS) is prosopagnosic but shows no covert recognition. The second (ME) is not prosopagnosic, but cannot access semantic information relating to familiar people. The model provides an account of recognition impairments which is sufficiently general also to be useful in describing these patients.     

Voice recognition and the posterior cingulate: An fMRI study of prosopagnosia

Voices, in addition to faces, enable person identification. Voice recognition has been shown to evoke a distributed network of brain regions that includes, in addition to the superior temporal sulcus (STS), the anterior temporal pole, fusiform face area (FFA), and posterior cingulate gyrus (pCG). Here we report an individual (MS) with acquired prosopagnosia who, despite bilateral damage to much of this network, demonstrates the ability to distinguish voices of several well‐known acquaintances from voices of people that he has never heard before. Functional magnetic resonance imaging (fMRI) revealed that, relative to speech‐modulated noise, voices rated as familiar and unfamiliar by MS elicited enhanced haemodynamic activity in the left angular gyrus, left posterior STS, and posterior midline brain regions, including the retrosplenial cortex and the dorsal pCG. More interestingly, relative to noise and unfamiliar voices, the familiar voices elicited greater haemodynamic activity in the left angular gyrus and medial parietal regions including the dorsal pCG and precuneus. The findings are consistent with theories implicating the pCG in recognizing people who are personally familiar, and furthermore suggest that the pCG region of the voice identification network is able to make functional contributions to voice recognition even though other areas of the network, namely the anterior temporal poles, FFA, and the right parietal lobe, may be compromised.     

Childhood prosopagnosia

K.D. has been unable to recognize people's faces since sustaining cerebral injury in infancy. Investigation of this disorder carried out when K.D. was aged 8 to 11 years showed that although her basic visual abilities were impaired, they were no poorer than those of other children who recognized faces without difficulty. K.D. had learned to read, but had not regained ability to recognize people's faces; instead she relied primarily on voices as a cue to person recognition. There was no evidence of any degree of overt or covert recognition of familiar faces, and K.D. also experienced problems in visual object recognition. She could, however, classify a visual input as a face, was able to perceive and imitate facial expressions, and was able to perform face matching tasks to an extent limited by her use of a feature by feature matching strategy. It is suggested that K.D.'s impairment affected higher order perceptual abilities, and is in a number of respects comparable to the impairments found in adult prosopagnosic patients.     

Face recognition and emotional valence: processing without awareness by neurologically intact participants does not simulate covert recognition in prosopagnosia

Covert face recognition in neurologically intact participants was investigated with the use of very brief stimulus presentation to prevent awareness of the stimulus. In Experiment 1, skin conductance response (SCR) to photographs of celebrity and unfamiliar faces was recorded; the faces were displayed for 220 msec and for 17 msec in a within-participants design. SCR to faces presented for 220 msec was larger and more likely to occur with familiar faces than with unfamiliar faces. Face familiarity did not affect the SCR to faces presented for 17 msec. SCR was larger for faces of good than for faces of evil celebrities presented for 17 msec, but valence did not affect SCR to faces displayed for 220 msec. In Experiment 2, associative priming was found in a face familiarity decision task when the prime face was displayed for 220 msec, but no facilitation occurred when primes were presented for 17 msec. In Experiment 3, participants were able to differentiate evil and good faces presented without awareness in a two-alternative forced-choice decision. The results provide no evidence of familiarity detection outside awareness in normal participants and suggest that, contrary to previous research, very brief presentation to neurologically intact participants is not a useful model for the types of covert recognition found in prosopagnosia. However, a response based on affective valence appears to be available from brief presentation.     

Perceptual functions in prosopagnosia

Some patients with prosopagnosia may have an apperceptive basis to their recognition defect. Perceptual abnormalities have been reported in single cases or small series, but the causal link of such deficits to prosopagnosia is unclear. Our goal was to identify candidate perceptual processes that might contribute to prosopagnosia, by subjecting several prosopagnosic patients to a battery of functions that may be necessary for accurate facial perception. We tested seven prosopagnosic patients. Three had unilateral right occipitotemporal lesions, two had bilateral posterior occipitotemporal lesions, and one had right anterior-to-occipital temporal damage along with a small left temporal lesion. These lesions all included the fusiform face area, in contrast to one patient with bilateral anterior temporal lesions. Most patients had impaired performance on face-matching tests and difficulty with subcategory judgments for non-face objects. The most consistent deficits in patients with lesions involving the fusiform face area were impaired perception of spatial relations in dot patterns and reduced contrast sensitivity in the 4 to 8 cycles deg(-1) range. Patients with bilateral lesions were impaired in saturation discrimination. Luminance discrimination was normal in all but two patients, and spatial resolution was uniformly spared. Curvature and line-orientation discrimination were impaired in only one patient, who also had the most difficulty with more basic-level object recognition. We conclude that deficits in luminance, spatial resolution, curvature, line orientation, and contrast at low spatial frequencies are unlikely to contribute to apperceptive prosopagnosia. More relevant may be contrast sensitivity at higher spatial frequencies and the analysis of object spatial structure. Deficits in these functions may impair perception of subtle variations in object shape, and may be one mechanism by which the recognition defect in prosopagnosia can extend to other classes of object subcategorization.     

Visual object agnosia without prosopagnosia or alexia: Evidence for hierarchical theories of visual recognition

Abstract

A single case study is presented of a patient, Mr. W, with a selective deficit in recognizing pictures and real objects, linked to impaired stored visual knowledge about objects. Despite this, Mr. W maintained a preserved ability both to read aloud printed words and to recognize famous faces, when compared with age-matched control subjects. In addition, his access to semantic information from words was superior to that from pictures. The data provide evidence that visual agnosia can occur without alexia or prosopagnosia, contrary to recent proposals (Farah 1990, 1991). This finding is consistent with a hierarchical model of visual object recognition in which agnosia can reflect impaired stored knowledge of objects without accompanying perceptual deficits. The selective recognition deficit for objects further indicates that stored knowledge concerning different classes of visual stimuli (common objects, faces, and words) is separately represented in the brain.     

Face gender recognition in developmental prosopagnosia: Evidence for holistic processing and use of configural information

Face identification deficits in developmental prosopagnosics (DPs) have been thought to be due to general difficulties with processing configural face information and integrating configural and parts information into a coherent whole (holistic processing). Gender recognition provides a further opportunity to more fully examine this issue as this ability may be intact in DPs and it has been shown to depend on processing configural information and holistic processing in neurotypical individuals. In the present study we first determined that, indeed, gender discrimination performance was similar in DPs and controls. Second, we found that inversion and scrambling (which we propose measures holistic processing and sensitivity to configural information, respectively) produced comparable deficits in DPs and controls, suggesting that both groups use holistic processing and configural information to recognize gender. This indicates that holistic processing and using configural face information are not general impairments in DP and may be more specific to face identity.     

Gaze behaviour in hereditary prosopagnosia

Prosopagnosia is the inability to recognize someone by the face alone in the absence of sensory or intellectual impairment. In contrast to the acquired form of prosopagnosia we studied the congenital form. Since we could recently show that this form is inherited as a simple monogenic trait we called it hereditary form. To determine whether not only face recognition and neuronal processing but also the perceptual acquisition of facial information is specific to prosopagnosia, we studied the gaze behaviour of four hereditary prosopagnosics in comparison to matched control subjects. This rarely studied form of prosopagnosia ensures that deficits are limited to face recognition. Whereas the control participants focused their gaze on the central facial features, the hereditary prosopagnosics showed a significantly different gaze behaviour. They had a more dispersed gaze and also fixated external facial features. Thus, the face recognition impairment of the hereditary prosopagnosics is reflected in their gaze behaviour.     

Implicit familiarity processing in congenital prosopagnosia

A particularly interesting and somewhat puzzling finding in the face‐processing literature is that, despite the absence of overt recognition of most faces, many patients with acquired prosopagnosia (AP) exhibit evidence of intact covert face recognition of the very same faces. This phenomenon has important implications for the understanding of the mechanism underlying AP and, by extension, the mechanism underlying normal face processing. Here, we set out to examine whether individuals with congenital prosopagnosia (CP) exhibit a similar dissociation between overt and covert face recognition. We first confirmed that all six of our CP individuals were significantly impaired in face recognition in comparison with controls. Participants then completed a matching task with both famous and unknown faces in which they decided whether two consecutive images have the same identity or not. Critically, the level of face familiarity was orthogonal to the task at hand and this enabled us to examine whether the familiarity of a face enhanced identity matching, a finding which would implicate implicit face processing. As expected, the CP individuals were slower and less accurate than the control participants. More importantly, like the controls, the CP individuals were faster and more accurate at matching famous compared with unknown faces. Also, for both groups, matching performance on unrecognized famous faces fell at an intermediate level between performance on explicitly recognized famous faces and faces which are unknown. These results provide the first solid evidence for the existence of implicit familiarity processing in CP and suggest that, despite the marked impairment in explicit face recognition, these individuals still have some familiarity representation which manifests in the form of covert recognition. We discuss possible models to account for the apparent dissociation of overt and covert face processing in CP.     

Developmental prosopagnosia: a review

This article reviews the published literature on developmental prosopagnosia, a condition in which the ability to recognize other persons by facial information alone has never been acquired. Due to the very low incidence of this syndrome, case reports are sparse. We review the available data and suggest assessment strategies for patients suffering from developmental prosopagnosia. It is suggested that developmental prosopagnosia is not a unitary condition but rather consists of different subforms that can be dissociated on the grounds of functional impairments. On the basis of the available evidence, hypotheses about the aetiology of developmental prosopagnosia as well as about the selectivity of deficits related to face recognition are discussed.     

Symptoms of prosopagnosia in intoxicated subjects.

Two experiments were made to test whether a blood ethanol concentration of about 1 g ethanol per kg blood influences the ability to recognize faces which were shown 24 hours earlier. 18 subjects who saw the faces for the first time when sober and whose task it was to recognize the faces when under the influence of alcohol, recognized the faces significantly less frequently than controls. The controls saw the faces for the first time when sober and their task was to recognize the faces later when also in a sober state. When 20 sober subjects had to recognize faces which they had seen 24 hours earlier under the influence of alcohol, they recognized the faces significantly less frequently than controls. 18 subjects to whom visual forms were shown when under the influence of alcohol and who had to recognize these forms 24 hours later when sober again performed like subjects who had to recognize faces under identical experimental conditions. Subjects who saw the forms, however, in a sober state and who had to recognize these forms when intoxicated performed significantly better than subjects who had to recognize faces under identical experimental conditions. In additional experiments, it was shown that alcohol did not influence ability to compare simultaneously presented faces. Intoxicated subjects' reduced abilities to recognize faces is regarded as a symptom of prosopagnosia since it cannot be explained by a reduced ability to recognize forms or to compare faces.     

Congenital prosopagnosia: face-blind from birth

Congenital prosopagnosia refers to the deficit in face processing that is apparent from early childhood in the absence of any underlying neurological basis and in the presence of intact sensory and intellectual function. Several such cases have been described recently and elucidating the mechanisms giving rise to this impairment should aid our understanding of the psychological and neural mechanisms mediating face processing. Fundamental questions include: What is the nature and extent of the face-processing deficit in congenital prosopagnosia? Is the deficit related to a more general perceptual deficit such as the failure to process configural information? Are any neural alterations detectable using fMRI, ERP or structural analyses of the anatomy of the ventral visual cortex? We discuss these issues in relation to the existing literature and suggest directions for future research.     

Thoughts provoked by pain

Despite the growing interest in the cognitive component of chronic pain, little information has been collected on the variety of thoughts provoked by pain experience. A new assessment instrument (the Cognitive Evaluative Questionnaire--CEQ) has been utilized with 127 chronic pain patients and their cognitions classified into seven discrete clusters. The results confirm the heterogeneity of pain cognitions, the majority of which are likely to play a role in enhancing or perpetuating chronic pain. The relationship of these cognitions to chronic avoidance behavior is discussed.     

Further observations on the nature of prosopagnosia

Two new cases of prosopagnosia are described and compared with pertinent clinical material from the English language literature. The interpretation of this disorder most compatible with the clinical data appears to us to be that there is an underspecification of visuoperceptive information preventing both the formation of significant face images and the retrieval of well-known face memoranda existing within a relatively intact visual remote memory store. Failure of formation of immediate memoranda of similarly complex visual images is also commonly observed but does not seem to be a requirement for the symptom of prosopagnosia. Conceptualizing this abnormality as simply a material specific visual agnosia of images beyond the classifier level would still appear to be acceptable if less informative.     

Electrodermal discrimination of familiar but not unfamiliar faces in prosopagnosia

It has been previously shown that prosopagnosics can electrodermally "recognize" faces they cannot verbally identify and with which they feel no familiarity. This study extended previous results by showing that electrodermal discrimination of faces exists only on a famous face identification task, and not on a matching-to-sample task involving unfamiliar faces. This suggests that electrodermal recognition reflects the activation of stored identity-specific information built up on the basis of past contact with faces, and provides a psychophysiological distinction between familiar and unfamiliar face processing. Implications for cognitive models of face recognition, and for understanding the nature of prosopagnosia, are discussed.