Covert processing of faces in prosopagnosia is restricted to facial expressions: evidence from cross-modal bias

We present a single case study of a brain-damaged patient, AD, suffering from visual face and object agnosia, with impaired visual perception and preserved mental imagery. She is severely impaired in all aspects of overt recognition of faces as well as in covert recognition of familiar faces. She shows a complete loss of processing facial expressions in recognition as well as in matching tasks. Nevertheless, when presented with a task where face and voice expressions were presented concurrently, there was a clear impact of face expressions on her ratings of the voice. The cross-modal paradigm used here and validated previously with normal subjects (de Gelder & Vroomen, 1995, 2000), appears as a useful tool in investigating spared covert face processing in a neuropsychological perspective, especially with prosopagnosic patients. These findings are discussed against the background of different models of the covert recognition of face expressions.     

Understanding provoked overt recognition in prosopagnosia

Prosopagnosic patients are unable to recognize overtly the faces of familiar people. However, under specific experimental conditions, overt recognition of faces has been induced in some prosopagnosics. This phenomenon of provoked overt recognition has proved challenging for current theories of face recognition. We first describe clinical demonstrations of provoked overt recognition, before highlighting some critical features that any satisfactory explanation of the phenomenon must accommodate. An account of provoked overt recognition is then put forward, couched within the framework of Burton, Bruce, and Johnston's (1990) IAC model of face recognition. This theory is tested by running computer simulations with the model. Finally, the present explanation of provoked overt recognition is scrutinized to discover whether it has implications for rehabilitation work with prosopagnosic patients.     

Cross-domain semantic priming in normal subjects and a prosopagnosic patient

Cross-domain semantic priming of person recognition (from face primes to name targets at 500msecs SOA) is investigated in normal subjects and a brain-injured patient (PH) with a very severe impairment of overt face recognition ability. Experiment 1 demonstrates equivalent semantic priming effects for normal subjects from face primes to name targets (cross-domain priming) and from name primes to name targets (within-domain priming). Experiment 2 demonstrates cross-domain semantic priming effects from face primes that PH cannot recognize overtly. Experiment 3 shows that cross-domain semantic priming effects can be found for normal subjects when target names are repeated across all conditions. This (repeated targets) method is then used in Experiment 4 to establish that PH shows equivalent semantic priming to normal subjects from face primes which he is very poor at identifying overtly and from name primes which he can identify overtly. These findings demonstrate that automatic aspects of face recognition can remain intact even when all sense of overt recognition has been lost.     

Prosopagnosia: A reclassification

We report a quantitative investigation of three patients who presented with a profound prosopagnosia. They were tested on a series of tests of face perception, face recognition, and paired associate learning using faces. A patient with marked perceptual difficulties but no difficulty whatever in recognizing faces was tested as a control. The control patient's performance was as bad or worse on the tests of perception of faces, and it is concluded that impaired performance on tests of face perception does not contribute to difficulties in recognizing familiar faces. The major difference between the three prosopagnosic patients was the evidence of covert recognition in two of these cases but not in the third. We use this evidence to argue that the perceptual/mnestic distinction is an inappropriate classification and would suggest instead that the two types may be described in terms either of a disconnection of the face recognition units or of damage to the units themselves.     

The biasing of figure-ground assignment by shading cues for objects and faces in prosopagnosia

Prosopagnosia is defined by impaired recognition of the identity of specific faces. Whether the perception of faces at the categorical level (recognizing that a face is a face) is also impaired to a lesser degree is unclear. We examined whether prosopagnosia is associated with impaired detection of facial contours in a bistable display, by testing a series of five prosopagnosic patients on a variation of Rubin's vase illusion, in which shading was introduced to bias perception towards either the face or the vase. We also included a control bistable display in which a disc or an aperture were the two possible percepts. With the control disc/aperture test, prosopagnosic patients did not generate a normal sigmoid function, but a U-shaped function, indicating that they perceived the shading but had difficulty in using the shading to make the appropriate figure-ground assignment. While controls still generated a sigmoid function for the vase/face test, prosopagnosic patients showed a severe impairment in using shading to make consistent perceptual assignments. We conclude that prosopagnosic patients have difficulty in using shading to segment figures from background correctly, particularly with complex stimuli like faces. This suggests that a subtler defect in face categorization accompanies their severe defect in face identification, consistent with predictions of computational models and recent data from functional imaging.     

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.     

Is the Right Anterior Temporal Variant of Prosopagnosia a Form of ‘Associative Prosopagnosia’ or a Form of ‘Multimodal Person Recognition Disorder’?

The construct of associative prosopagnosia is strongly debated for two main reasons. The first is that, according to some authors, even patients with putative forms of associative visual agnosia necessarily present perceptual defects, that are the cause of their recognition impairment. The second is that in patients with right anterior temporal lobe (ATL) lesions (and sparing of the occipital and fusiform face areas), who can present a defect of familiar people recognition, with normal results on tests of face perception, the disorder is often multimodal, affecting voices (and to a lesser extent names) in addition to faces. The present review was prompted by the claim, recently advanced by some authors, that face recognition disorders observed in patients with right ATL lesions should be considered as an associative or amnestic form of prosopagnosia, because in them both face perception and retrieval of personal semantic knowledge from name are spared. In order to check this claim, we surveyed all the cases of patients who satisfied the criteria of associative prosopagnosia reported in the literature, to see if their defect was circumscribed to the visual modality or also affected other channels of people recognition. The review showed that in most patients the study had been limited to the visual modality, but that, when the other modalities of people recognition had been taken into account, the defect was often multimodal, affecting voice (and to a lesser extent name) in addition to face.     

Reduced fixation on the upper area of personally familiar faces following acquired prosopagnosia

Selective impairment of face recognition following brain damage, as in acquired prosopagnosia, may cause a dramatic loss of diagnosticity of the eye area of the face and an increased reliance on the mouth for identification ( Caldara et al., 2005 ). To clarify the nature of this phenomenon, we measured eye fixation patterns in a case of pure prosopagnosia (PS, Rossion et al., 2003 ) during her identification of photographs of personally familiar faces (27 children of her kindergarten). Her age‐matched colleague served as a control. Consistent with previous evidence, the normal control identified the faces within two fixations located just below the eyes (central upper nose). This pattern (location and duration) of fixations remained unchanged even by increasing difficulty by presenting anti‐caricatures of the faces. In contrast, the great majority of the patient's fixations, irrespective of her accuracy, were located on the mouth. Overall, these observations confirm the abnormally reduced processing of the upper area of the face in acquired prosopagnosia. Most importantly, the prosopagnosic patient also fixated the area of the eyes spontaneously in between the first and last fixation, ruling out alternative accounts of her behaviour such as, for example, avoidance or failure to orient attention to the eyes, as observed in autistic or bilateral amygdala patients. Rather, they reinforce our proposal of a high‐level perceptual account ( Caldara et al., 2005 ), according to which acquired prosopagnosic patients have lost the ability to represent multiple elements of an individual face as a perceptual unit (holistic face perception). To identify a given face, they focus very precisely on local features rather than seeing the whole of a face from its diagnostic centre (i.e. just below the eyes). The upper area of the face is particularly less attended to and less relevant for the prosopagnosic patient because it contains multiple features that require normal holistic perception in order to be the most diagnostic region. Consequently, prosopagnosic patients develop a more robust representation of the mouth, a relatively isolated feature in the face that may contain more information than any single element of the upper face area, and is thus sampled repeatedly for resolving ambiguity in the process of identification.     

What is Overt and what is Covert in Congenital Prosopagnosia?

The term covert recognition refers to recognition without awareness. In the context of face recognition, it refers to the fact that some individuals show behavioural, electrophysiological or autonomic indices of recognition in the absence of overt, conscious recognition. Originally described in cases of people that have lost their ability to overtly recognize faces (acquired prosopagnosia, AP), covert face recognition has more recently also been described in cases of congenital prosopagnosia (CP), who never develop typical overt face recognition skills. The presence of covert processing in a developmental disorder such as CP is a particularly intriguing phenomenon, and its investigation is relevant for a variety of reasons. From a theoretical point of view, it is useful to help shed light on the cognitive and neural underpinnings of face recognition deficits. From a clinical point of view, it has the potential to aid the design of rehabilitation protocols aimed at improving face recognition skills in this population. In the current review we selectively summarize the recent literature on covert face recognition in CP, highlight its main findings, and provide a theoretical interpretation for them.     

Capgras delusion: a window on face recognition

Capgras delusion is the belief that significant others have been replaced by impostors, robots or aliens. Although it usually occurs within a psychiatric illness, it can also be the result of brain injury or other obviously organic disorder. In contrast to patients with prosopagnosia, who cannot consciously recognize previously familiar faces but display autonomic or covert recognition (measured by skin conductance responses), people with Capgras delusion do not show differential autonomic activity to familiar compared with unknown faces. This challenges traditional models of the way faces are identified and presents some epistemological questions concerning identity. New data also indicate that, contrary to previous evidence, covert recognition can be fractionated into autonomic and behavioural/cognitive types, which is consistent with a recently proposed modification of the modal face recognition model.     

Structure and function in acquired prosopagnosia: Lessons from a series of 10 patients with brain damage

Acquired prosopagnosia varies in both behavioural manifestations and the location and extent of underlying lesions. We studied 10 patients with adult‐onset lesions on a battery of face‐processing tests. Using signal detection methods, we found that discriminative power for the familiarity of famous faces was most reduced by bilateral occipitotemporal lesions that involved the fusiform gyri, and better preserved with unilateral right‐sided lesions. Tests of perception of facial structural configuration showed severe deficits with lesions that included the right fusiform gyrus, whether unilateral or bilateral. This deficit was most consistent for eye configuration, with some patients performing normally for mouth configuration. Patients with anterior temporal lesions had better configuration perception, though at least one patient showed a more subtle failure to integrate configural data from different facial regions. Facial imagery, an index of facial memories, was severely impaired by bilateral lesions that included the right anterior temporal lobe and marginally impaired by fusiform lesions alone; unilateral right fusiform lesions tended to spare imagery for facial features. These findings suggest that (1) prosopagnosia is more severe with bilateral than unilateral lesions, indicating a minor contribution of the left hemisphere to face recognition, (2) perception of facial configuration critically involves the right fusiform gyrus and (3) access to facial memories is most disrupted by bilateral lesions that also include the right anterior temporal lobe. This supports assertions that more apperceptive variants of prosopagnosia are linked to fusiform damage, whereas more associative variants are linked to anterior temporal damage. Next, we found that behavioural indices of covert recognition correlated with measures of overt familiarity, consistent with theories that covert behaviour emerges from the output of damaged neural networks, rather than alternative pathways. Finally, to probe the face specificity of the prosopagnosic defect, we tested recognition of fruits and vegetables: While face specificity was not found in most of our patients, the data of one patient suggested that this may be possible with more focal lesions of the right fusiform gyrus.     

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.     

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.     

The role of holistic face processing in acquired prosopagnosia: evidence from the composite face effect

Faces are processed more holistically than other objects, and it has been suggested that the loss of holistic face processing causes acquired prosopagnosia. Support for this hypothesis comes from several cases who failed to show holistic face effects as well as the absence of reports of prosopagnosics with unequivocally normal holistic face perception. The current study examines the relationship between holistic face processing and prosopagnosia by testing seven acquired prosopagnosics with the face composite task, a classic measure of holistic face processing. To enhance the robustness of the findings, each prosopagnosic was tested with two versions of the composite task showing upright faces. We also tested an inverted condition to exclude the possibility that more general factors account for composite effects for upright faces. Four of the seven acquired prosopagnosic participants showed consistent upright face composite effects with minimal inverted face composite effects. We conclude that severe face processing deficits can co-occur with intact holistic face processing and that factors other than a loss of holistic processing contribute to the perceptual and recognition deficits in acquired prosopagnosia.     

Access to identity-specific semantic codes from familiar faces

Information codes that can specify the surface form of a face are contrasted with semantic codes describing the properties of the person to whom the face belongs. Identity-specific semantic codes that specify characteristics of familiar people based on personal knowledge are in turn contrasted with the visually derived semantic codes and expression codes that can be derived even from unfamiliar faces. The idea that familiarity decisions (i.e., categorizing faces as belonging to known or unknown people) can be based on surface form, whereas certain types of semantic decision demand additional access to identity-specific semantic codes was investigated in four experiments. Experiments 1 and 3 showed that decisions based on identity-specific semantic codes (semantic decisions) usually take longer than decisions that do not demand access to an identity-specific semantic code (familiarity decisions). Experiment 2 showed that the use of familiar faces drawn from consistent or mixed categories affected reaction times for semantic decisions but not for familiarity decisions. Experiment 4 showed that semantic decisions to faces are taken more quickly (primed) when the faces have been recently seen, whereas there is no differential effect on semantic decisions to faces from previous semantic decisions involving the same people's names. These findings are consistent with the view that identity-specific semantic codes are accessed via face recognition units, and that outputs from face recognition units (which respond to the face's surface form) can be used as the basis for familiarity decisions.     

Is the loss of diagnosticity of the eye region of the face a common aspect of acquired prosopagnosia?

A recent study published in this journal has shown an abnormal performance at discriminating differences with respect to the eyes of unfamiliar faces in two acquired prosopagnosic patients, but preserved processing of the mouth region. Here we extend these findings by showing a similar lack of sensitivity to the eyes in the very same face matching experiment for the prosopagnosic patient PS, who also showed normal performance for detecting differences in the mouth region. These results complement previously published evidence that the patient PS presents a lack of sensitivity to diagnostic information located on the eyes of familiar faces during individual face recognition tasks. More generally, they indicate that the impaired processing of the eyes of faces is a fundamental aspect of acquired prosopagnosia that can arise following damage to different brain localizations.     

Covert face recognition in neurologically intact participants

Prosopagnosic patients may maintain some ability to recognize familiar faces, although they remain unaware of this ability. This phenomenon – called covert face recognition – was investigated in neurologically intact participants, using priming techniques. Participants were quicker to indicate that a target-name was familiar when the preceding prime-face belonged to the same person compared with an unrelated familiar person. This was observed both when prime-faces could be recognized overtly and when they were presented too briefly to be recognized overtly (Exps. 1 and 2). Thus, covert face recognition was observed in neurologically intact participants. In Exp. 3, participants were quicker to recognize a familiar face when that person's face had been seen previously, but only when it had been recognized overtly on the first encounter. These results are interpreted within the framework of an interactive activation model of face recognition. Received: 21 September 1998 / Accepted: 2 March 1999     

Neuropsychological Impairment of Face Recognition Units

Despite the absence of “conscious”, overt identification, some patients with face recognition impairments continue covertly to process information regarding face familiarity. The fact that by no means all patients show these covert effects has led to the suggestion that indirect recogntion tasks may help in identifying different types of face recognition impairment. The present report describes a number of experiments with the patient NR, who, after a closed head injury, has been severely impaired at recognizing familiar faces. Investigations mostly failed to show overt or covert face recognition, but NR performed at an above-chance level in selecting the familiar face on a task requiring a forced-choice between a familiar and an unfamiliar face. This discrepancy between a degree of rudimentary overt recognition and absence of covert effects on most indirect tests was addressed using a cross-domaim identity priming paradigm. This examined separately the possibility of preserved recognition for faces that NR consistently chose correctly in a forced-choice familiarity decision and those on which he performed at chance level. Priming effects were apparent only for the faces that were consistently chosen as “familiar” in forced-choice. We suggest that NR's stored representations of familiar faces are degraded, so that face recognition is possible only via a limited set of relatively preserved representations able to support a rudimentary form of overt recognition and to facilitate performance in matching and priming tasks.     

Beyond localisation: a dynamical dual route account of face recognition

After decades of research the notion that faces are special is still at the heart of heated debates. New techniques like brain imaging have advanced some of the arguments but empirical data from brain-damaged patients like paradoxical recognition effects have required more complex explanations aside from localisation of the face area in normal adults. In this paper we focus on configural face processes and discuss configural processes in prosopagnosics in the light of findings obtained in brain-imaging studies. In order to account for data like paradoxical face recognition effects we propose a dual route model of face recognition. The model is based on the distinction between two separate aspects of face recognition, detection and identification, considered as dynamical and interrelated. In this perspective the face detection system appears as the stronger candidate for face-specific processes. The face identification system on the other hand is part of the object recognition system but derives its specificity in part from interaction with the face-specific detection system. The fact that face detection appears intact in some patients provides us with a possible explanation for the interference of configural processes on feature-based identification.     

Spreading Activation in an Attractor Network With Latching Dynamics: Automatic Semantic Priming Revisited

Localist models of spreading activation (SA) and models assuming distributed representations offer very different takes on semantic priming, a widely investigated paradigm in word recognition and semantic memory research. In this study, we implemented SA in an attractor neural network model with distributed representations and created a unified framework for the two approaches. Our models assume a synaptic depression mechanism leading to autonomous transitions between encoded memory patterns (latching dynamics), which account for the major characteristics of automatic semantic priming in humans. Using computer simulations, we demonstrated how findings that challenged attractor‐based networks in the past, such as mediated and asymmetric priming, are a natural consequence of our present model’s dynamics. Puzzling results regarding backward priming were also given a straightforward explanation. In addition, the current model addresses some of the differences between semantic and associative relatedness and explains how these differences interact with stimulus onset asynchrony in priming experiments.