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.     

Developmental prosopagnosia: a study of three patients

We studied perception in three patients with prosopagnosia of childhood onset. All had trouble with other 'within-category' judgments. All were deficient on face matching tests and severely impaired on tests of perception of the spatial relations of facial features and abstract designs, indicating a deficit in the encoding of coordinate relationships, similar to adult-onset prosopagnosia with lesions of the fusiform face area. Two had difficulty perceiving feature colour, which correlated with reduced luminance sensitivity. In contrast to adult-onset patients, saturation discrimination was spared in two and spatial resolution impaired in two. Curvature discrimination was relatively spared. Contrast sensitivity showed variable reductions at different spatial frequencies. We conclude that developmental prosopagnosia is similar to the adult-onset form in encoding deficits for the spatial arrangement of facial elements. Deficits in luminance perception and spatial resolution are more associated with defective encoding for basic object-level recognition, as shown on tests of object and spatial perception.     

Dissociation between the effects of damage to perirhinal cortex and area TE

Perirhinal cortex and area TE are immediately adjacent to each other in the temporal lobe and reciprocally interconnected. These areas are thought to lie at the interface between visual perception and visual memory, but it has been unclear what their separate contributions might be. In three experiments, monkeys with bilateral lesions of the perirhinal cortex exhibited a different pattern of impairment than monkeys with bilateral lesions of area TE. In experiment 1, lesions of the perirhinal cortex produced a multimodal deficit in recognition memory (delayed nonmatching to sample), whereas lesions of area TE impaired performance only in the visual modality. In experiment 2, on a test of visual recognition memory (the visual paired comparison task) lesions of the perirhinal cortex impaired performance at long delays but spared performance at a very short delay. In contrast, lesions of area TE impaired performance even at the short delay. In experiment 3, lesions of the perirhinal cortex and lesions of area TE produced an opposite pattern of impairment on two visual discrimination tasks, simple object discrimination learning (impaired only by perirhinal lesions), and concurrent discrimination learning (impaired only by TE lesions). Taken together, the findings suggest that the perirhinal cortex, like other medial temporal lobe structures, is important for the formation of memory, whereas area TE is important for visual perceptual processing.     

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.     

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.     

Perirhinal cortex resolves feature ambiguity in configural object recognition and perceptual oddity tasks

The perirhinal cortex (PRh) has a well-established role in object recognition memory. More recent studies suggest that PRh is also important for two-choice visual discrimination tasks. Specifically, it has been suggested that PRh contains conjunctive representations that help resolve feature ambiguity, which occurs when a task cannot easily be solved on the basis of features alone. However, no study has examined whether the ability of PRh to resolve configural feature ambiguity is related to its role in object recognition. Therefore, we examined whether bilateral excitotoxic lesions of PRh or PPRh (perirhinal plus post-rhinal cortices) in the rat would cause deficits in a configural spontaneous object recognition task, and a configural simultaneous oddity discrimination task, in which the task could not be solved on the basis of features, but could only be solved using conjunctive representations. As predicted by simulations using a computational model, rats with PPRh lesions were impaired during a minimal-delay configural object recognition task. These same rats were impaired during a zero-delay configural object recognition task. Furthermore, rats with localized PRh lesions were impaired in a configural simultaneous oddity discrimination task. These findings support the idea that PRh contains conjunctive representations for the resolution of feature ambiguity and that these representations underlie a dual role for PRh in memory and perception.     

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 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.     

TMS to the “occipital face area” affects recognition but not categorization of faces

The human cortical system for face perception is comprised of a network of connected regions including the middle fusiform gyrus (“fusiform face area” or FFA), the inferior occipital cortex (“occipital face area” or OFA), and the superior temporal sulcus. The traditional hierarchical feedforward model of visual processing suggests information flows from early visual cortex to the OFA for initial face feature analysis to higher order regions including the FFA for identity recognition. However, patient data suggest an alternative model. Patients with acquired prosopagnosia, an inability to visually recognize faces, have been documented with lesions to the OFA but who nevertheless show face-selective activation in the FFA. Moreover, their ability to categorize faces remains intact. This suggests that the FFA is not solely responsible for face recognition and the network is not strictly hierarchical, but may be organized in a reverse hierarchical fashion. We used transcranial magnetic stimulation (TMS) to temporarily disrupt processing in the OFA in neurologically-intact individuals and found participants’ ability to categorize intact versus scrambled faces was unaffected, however face identity discrimination was significantly impaired. This suggests that face categorization but not recognition can occur without the “earlier” OFA being online and indicates that “lower level” face category processing may be assumed by other intact face network regions such as the FFA. These results are consistent with the patient data and support a non-hierarchical, global-to-local model with re-entrant connections between the OFA and other face processing areas.     

Preservation of mouth region processing in two cases of prosopagnosia

Although most adults are considered experts in face recognition, brain trauma can produce a selective loss in this ability, a condition referred to as prosopagnosia. This study examined the processing strategies of prosopagnosic patients LR and HH using the Face Dimensions Test. In this test, featural and configural information in the upper and lower halves of the face was parametrically varied and sensitivity to these changes measured. We found that relative to age‐matched control participants, LR and HH exhibited an impaired ability to discriminate differences in the eye region, but a preserved ability to detect featural and configural differences in the mouth region. This pattern of impairment and sparing was demonstrated in tests of direct perception and immediate memory. The obtained findings demonstrate that prosopagnosia does not necessarily cause a global impairment to face perception, but a selective impairment to the perception of information in the upper half of the face.     

TMS to the “occipital face area” affects recognition but not categorization of faces

The human cortical system for face perception is comprised of a network of connected regions including the middle fusiform gyrus (“fusiform face area” or FFA), the inferior occipital cortex (“occipital face area” or OFA), and the superior temporal sulcus. The traditional hierarchical feedforward model of visual processing suggests information flows from early visual cortex to the OFA for initial face feature analysis to higher order regions including the FFA for identity recognition. However, patient data suggest an alternative model. Patients with acquired prosopagnosia, an inability to visually recognize faces, have been documented with lesions to the OFA but who nevertheless show face-selective activation in the FFA. Moreover, their ability to categorize faces remains intact. This suggests that the FFA is not solely responsible for face recognition and the network is not strictly hierarchical, but may be organized in a reverse hierarchical fashion. We used transcranial magnetic stimulation (TMS) to temporarily disrupt processing in the OFA in neurologically-intact individuals and found participants’ ability to categorize intact versus scrambled faces was unaffected, however face identity discrimination was significantly impaired. This suggests that face categorization but not recognition can occur without the “earlier” OFA being online and indicates that “lower level” face category processing may be assumed by other intact face network regions such as the FFA. These results are consistent with the patient data and support a non-hierarchical, global-to-local model with re-entrant connections between the OFA and other face processing areas.     

Further lesion evidence for the neural basis of conceptual knowledge for persons and other concrete entities

The neural underpinnings of conceptual knowledge have been studied intensively, but many unanswered questions remain. In a previous study examining recognition of persons, animals, and tools in 116 participants with unilateral brain lesions, we found no instance of a patient who manifested defective recognition in all three categories. We reasoned that the spatial distribution of the lesion loci critical for the appearance of recognition defects for these different categories explained why this ‘three‐way’ defect could not be found in patients with unilateral lesions, and we proposed that only a suitable bilateral lesion would be likely to produce such a combined defect. In the study reported here, we tested this hypothesis by investigating recognition performances in 55 participants with bilateral cortical lesions. In support of the hypothesis, nine patients, all of whose lesions included bilateral occipitotemporal and/or temporal cortices, had a three‐way recognition impairment (persons, M=18.3%; animals, M=35.7%; tools, M=71.3%; all scores >2 SDs below normal). As expected, bilateral lesions to other neural sectors, for example prefrontal cortices, did not lead to recognition impairments. These findings provide further support for the notion that retrieval of knowledge for concrete entities from different conceptual categories depends on partially segregated neural systems, located in different sectors of occipitotemporal and temporal regions in right and left hemisphere.     

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.     

Memory and executive function impairments after frontal or posterior cortex lesions

Free recall and recognition, memory for temporal order, spatial memory and prospective memory were assessed in patients with frontal lobe lesions, patients with posterior cortex lesions and control subjects. Both patient groups showed equivalent memory deficits relative to control subjects on a range of free recall and recognition tasks, on memory for temporal order and on a prospective memory task. The patient groups also performed equivalently on the spatial memory task although only patients with frontal lobe lesions were significantly impaired. However, the patients with frontal lobe lesions showed an increased false alarm rate and made more intrusion errors relative not only to the control subjects, but also to the patients with poster or cortex lesions. These memory problems are discussed in relation to deficits in executive function and basic memory processes.     

Object Recognition Difficulty in Visual Apperceptive Agnosia

Two patients with visual apperceptive agnosia were examined on tasks assessing the appreciation of visual material. Elementary visual functioning was relatively preserved, but they had profound difficulty recognizing and naming line drawings. More detailed evaluation revealed accurate recognition of regular geometric shapes and colors, but performance deteriorated when the shapes were made more complex visually, when multiple-choice arrays contained larger numbers of simple targets and foils, and when a mental manipulation such as a rotation was required. The recognition of letters and words was similarly compromised. Naming, recognition, and anomaly judgments of colored pictures and real objects were more accurate than similar decisions involving black-and-white line drawings. Visual imagery for shapes, letters, and objects appeared to be more accurate than visual perception of the same materials. We hypothesize that object recognition difficulty in visual apperceptive agnosia is due to two related factors: the impaired appreciation of the visual perceptual features that constitute objects, and a limitation in the cognitive resources that are available for processing demanding material within the visual modality.     

Intact visual discrimination of complex and feature-ambiguous stimuli in the absence of perirhinal cortex

The perirhinal cortex is known to be important for memory, but there has recently been interest in the possibility that it might also be involved in visual perceptual functions. In four experiments, we assessed visual discrimination ability and visual discrimination learning in severely amnesic patients with large medial temporal lobe lesions that included complete lesions of perirhinal cortex. Experiment 1 tested complex visual object perception. Experiments 2a and 2b tested in two different ways the ability to discriminate between feature-ambiguous images, which was reported to be impaired in monkeys with perirhinal lesions. Experiment 3 involved images that were successfully discriminated in Experiment 2a and asked patients to learn across 20 trials which of the images had been designated as "correct." Patients performed as well as controls in Experiments 1, 2a, and 2b, but one of the patients had difficulty in Experiment 3 when the task required remembering from trial to trial which image was "correct." These findings indicate that perirhinal cortex is not needed for visual perception across a wide range of visual perceptual tasks.     

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.     

发展性面孔失认的认知机制及其神经基础

发展性面孔失认症是指个体在童年期就开始表现出来的一种终生性面孔识别缺陷,其不能归因于智力衰退、情感障碍、物体识别困难以及后天性脑损伤.发展性面孔失认症涉及的认知机制包括面孔特异性机制、构型加工障碍、面孔探测、面孔记忆和面孔身份识别.此外,该面孔失认症的神经网络由核心神经网络和延伸的神经网络组成,前者与面孔选择反应和记忆表征有关,后者主要负责面孔知识表征、面孔长时记忆和面孔工作记忆.今后的研究应集中在完善延伸的神经网络、拓展其认知网络;进一步明确面孔探测与发展性面孔失认之间的关系;考察发展性面孔失认症的基因基础、加强其发展性研究以及推动康复工作的展开.     

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 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.