A case of prosopagnosia following moderate closed head injury with left hemisphere focal lesion

This study describes a left handed woman with prosopagnosia following traumatic brain injury with a focal lesion confined to the left-posterior hemisphere. Few cases of prosopagnosia following unilateral left hemisphere lesions have previously been reported in the literature. Corrected visual acuity was 20/70 (binocular), color vision was intact on screening, and shape detection was borderline. Impairments in higher order visual perception were evident to varying degrees on nonfacial tasks. Matching of unfamiliar faces was very slow but accurate. A marked impairment in the ability to recognize familiar faces and learn new face-name associations was evident on experimental tasks relative to the performance of healthy control subjects. In contrast, identification of characteristics of faces (gender, age) and identification and matching of facial expressions were relatively preserved. We discuss the cognitive processing stages that appear to be disrupted using Bruce and Young's (1986) model of facial recognition and perception as a framework.     

Selective impairment of facial recognition due to a haematoma restricted to the right fusiform and lateral occipital region

A 67 year old right handed Japanese man developed prosopagnosia caused by a haemorrhage. His only deficit was the inability to perceive and discriminate unfamiliar faces, and to recognise familiar faces. He did not show deficits in visual or visuospatial perception of non-facial stimuli, alexia, visual agnosia, or topographical disorientation. Brain MRI showed a haematoma limited to the right fusiform and the lateral occipital region. Single photon emission computed tomography confirmed that there was no decreased blood flow in the opposite left cerebral hemisphere. The present case indicates that a well placed small right fusiform gyrus and the adjacent area can cause isolated impairment of facial recognition. As far as we know, there has been no published case that has demonstrated this exact lesion site, which was indicated by recent functional MRI studies as the most critical area in facial recognition.     

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.     

Lesions of the fusiform face area impair perception of facial configuration in prosopagnosia.

BACKGROUND: Prosopagnosia, the inability to recognize faces, is associated with medial occipitotemporal lesions, especially on the right. Functional imaging has revealed a focal region in the right fusiform gyrus activated specifically during face perception. OBJECTIVE: The study attempted to determine whether lesions of this region were associated with defects in face perception in patients with prosopagnosia. METHODS: Five patients with acquired prosopagnosia were tested. They were asked to discriminate faces in which the spatial configuration of features had been altered. This was contrasted with their discrimination of changes in feature color, an alteration that does not affect spatial relations. RESULTS: All four patients whose lesions included the right fusiform face area were severely impaired in discriminating changes in the spatial position of features. The one patient with anterior bilateral lesions was normal in this perceptual ability. For three of the five patients, accuracy was normal for changes in eye color. When subjects knew that only changes in mouth position would be shown, performance improved markedly in two of the four patients who were impaired in the initial test. CONCLUSION: Perception of facial configuration is impaired in patients with prosopagnosia whose lesions involve the right fusiform gyrus. This deficit is especially manifest when attention must be distributed across numerous facial elements. It does not occur with more anterior bilateral temporal lesions. Loss of this ability may contribute to the recognition defect in some forms of prosopagnosia.     

The anatomical basis of prosopagnosia

Evidence is presented that patients with prosopagnosia have right anterior inferior occipital lesions in the region of the occipital temporal junction. Many if not all cases have an additional lesion in the left hemisphere; this is often but apparently not always symmetrical with the right hemisphere lesion. This evidence is discussed in relation to the anatomical connections of these regions and the results of experiments in animals.     

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.     

Double disconnection effects resulting from infiltrating tumors

Patients with left hemisphere lesions deep in parietal or parietal-occipital regions close to the lateral ventricles have been reported to have impaired performance on left ear speech stimuli in dichotic listening tests. This loss has been termed "paradoxical" because it presents at the ear ipsilateral to the lesion. Two patients with infiltrating tumors which involved the corpus callosum demonstrated that effect, but also demonstrated right ear extinction on a complex-pitch discrimination test that required right hemisphere processing. Since the side at which the impairment will be demonstrated depends upon the type of test used, the term "paradoxical extinction" does not clearly describe this phenomena. It is suggested that the so-called paradoxical loss is better referred to as callosal extinction.     

Are unilateral right posterior cerebral lesions sufficient to cause prosopagnosia? Clinical and radiological findings in six additional patients

Controversy has arisen regarding the neuropathological basis of prosopagnosia. Some investigators suggest that bilateral lesions are needed to cause the deficit, whereas others felt that a unilateral right posterior lesion is sufficient. Six patients with prosopagnosia with clinical and radiological evidence of unilateral right posterior lesions are presented. Our observations together with evidence from similar cases described in the literature suggest that an appropriately placed right hemispheric lesion may be sufficient to produce prosopagnosia.     

Prosopagnosia: a clinical,psychological, and anatomical study of three patients.

Three patients with prosopagnosia are described of whom two had right occipital lesions. An analysis of visual and perceptual functions demonstrated a defect in perceptual classification which appeared to be stimulus-specific. A special mechanism for facial recognition is postulated, and the importance of the right sided posterior lesion is stressed.     

Neural mechanisms of facial recognition]

We review recent researches in neural mechanisms of facial recognition in the light of three aspects: facial discrimination and identification, recognition of facial expressions, and face perception in itself. First, it has been demonstrated that the fusiform gyrus has a main role of facial discrimination and identification. However, whether the FFA (fusiform face area) is really a special area for facial processing or not is controversial; some researchers insist that the FFA is related to 'becoming an expert' for some kinds of visual objects, including faces. Neural mechanisms of prosopagnosia would be deeply concerned to this issue. Second, the amygdala seems to be very concerned to recognition of facial expressions, especially fear. The amygdala, connected with the superior temporal sulcus and the orbitofrontal cortex, appears to operate the cortical function. The amygdala and the superior temporal sulcus are related to gaze recognition, which explains why a patient with bilateral amygdala damage could not recognize only a fear expression; the information from eyes is necessary for fear recognition. Finally, even a newborn infant can recognize a face as a face, which is congruent with the innate hypothesis of facial recognition. Some researchers speculate that the neural basis of such face perception is the subcortical network, comprised of the amygdala, the superior colliculus, and the pulvinar. This network would relate to covert recognition that prosopagnosic patients have.     

Lateralisation of perceptual processing of pro- and anti-social emotions displayed in chimeric faces

Previous studies using a restricted range of split field chimeric faces suggest that the processing of facial emotional expressions is a highly lateralised phenomenon. Two theories have emerged with regard to the role the two cerebral hemispheres play in this processing. The "right hemisphere" hypothesis (e.g. Borod, Koff, Lorch, & Nicholas, 1988) suggests that the right hemisphere plays a prominent role in the processing of both positive and negative facial expressions. In contrast, the "valence hypothesis" (e.g. Reuter-Lorenz & Davidson, 1981) proposes that, while the right hemisphere plays the major role in processing negative emotions, the left hemisphere has a special role for positive emotions. Using all six of the human "universal facial expressions" (Ekman &Friesen, 1971) we present evidence that, superimposed onto a left visual field advantage (right hemisphere specialisation) for emotional processing, there is a "left shift" (right visual field advantage) for pro- as opposed to anti-social expression. We propose that facial expressions that are likely to be related to approach for communicative purposes initiate a greater degree of left hemisphere involvement. As a consequence, we suggest that for future laterality studies, the six universal emotional expressions should be reconsidered using a pro- to anti-social dimension rather than positive and negative groupings.     

Lateralisation of perceptual processing of pro- and anti-social emotions displayed in chimeric faces

Previous studies using a restricted range of split field chimeric faces suggest that the processing of facial emotional expressions is a highly lateralised phenomenon. Two theories have emerged with regard to the role the two cerebral hemispheres play in this processing. The "right hemisphere" hypothesis (e.g. Borod, Koff, Lorch, & Nicholas, 1988) suggests that the right hemisphere plays a prominent role in the processing of both positive and negative facial expressions. In contrast, the "valence hypothesis" (e.g. Reuter-Lorenz & Davidson, 1981) proposes that, while the right hemisphere plays the major role in processing negative emotions, the left hemisphere has a special role for positive emotions. Using all six of the human "universal facial expressions" (Ekman &Friesen, 1971) we present evidence that, superimposed onto a left visual field advantage (right hemisphere specialisation) for emotional processing, there is a "left shift" (right visual field advantage) for pro- as opposed to anti-social expression. We propose that facial expressions that are likely to be related to approach for communicative purposes initiate a greater degree of left hemisphere involvement. As a consequence, we suggest that for future laterality studies, the six universal emotional expressions should be reconsidered using a pro- to anti-social dimension rather than positive and negative groupings.     

Alterations of the sense of "humanness" in right hemisphere predominant frontotemporal dementia patients.

OBJECTIVE: To evaluate the sense of "humanness" in frontotemporal dementia (FTD) patients with right hemispheric involvement. BACKGROUND: Early in the course, FTD is often asymmetric, and those with predominant right frontotemporal disease have disproportionate disturbances in social behavior and empathy. A disruption in a sense of humanness may underlie these behavioral disturbances. METHOD: Sixteen patients with asymmetric FTD on functional neuroimaging underwent recognition tests of facial masking, human-animal morphing, and facial distortion. Additional tests evaluated facial discrimination and the recognition of famous faces, facial emotions, and animate-inanimate differences. RESULTS: On the distorted and morphed face tasks, 8 FTD patients with predominant right hemisphere involvement were significantly more likely to call morphed and distorted faces "human" as compared with both 8 FTD patients with predominant left hemisphere involvement and normal controls. The FTD groups did not differ on thresholds for recognizing masked faces or on other face recognition measures. CONCLUSIONS: In FTD, right hemispheric involvement may alter the threshold for judging someone as human independent of the recognition of faces or facial affect. These results suggest that a specific sense of humanness facilitates a person recognition network in the right frontotemporal region of the brain.     

Prosopagnosia in two patients with CT scan evidence of damage confined to the right hemisphere

Two patients developed a severe and long-lasting inability to recognize familiar faces (prosopagnosia) after a stroke, which was shown by CT scan to be confined to the right hemisphere. The area of softening involved the entire cortico-subcortical territory of distribution of the right posterior cerebral artery. These data suggest that in a few cases right occipito-temporal damage may be sufficient to produce prosopagnosia.     

Perception of emotions from faces and voices following unilateral brain damage

The importance of the right hemisphere in emotion perception in general has been well documented but its precise role is disputed. We compared the performance of 30 right hemisphere damaged (RHD) patients, 30 left hemisphere damaged (LHD) patients, and 50 healthy controls on both facial and vocal affect perception tasks of specific emotions. Brain damaged subjects had a single episode cerebrovascular accident localised to one hemisphere. The results showed that right hemisphere patients were markedly impaired relative to left hemisphere and healthy controls on test performance: labelling and recognition of facial expressions and recognition of emotions conveyed by prosody. This pertained at the level of individual basic emotions, positive versus negative, and emotional expressions in general. The impairment remained highly significant despite covarying for the group's poorer accuracy on a neutral facial perception test and identification of neutral vocal expressions. The LHD group were only impaired relative to controls on facial emotion tasks when their performance was summed over all the emotion categories and before age and other cognitive factors were taken into account. However, on the prosody test the LHD patients showed significant impairment, performing mid-way between the right hemisphere patients and healthy comparison group. Recognition of positive emotional expressions was better than negative in all subjects, and was not relatively poorer in the LHD patients. Recognition of individual emotions in one modality correlated weakly with recognition in another, in all three groups. These data confirm the primacy of the right hemisphere in processing all emotional expressions across modalities--both positive and negative--but suggest that left hemisphere emotion processing is modality specific. It is possible that the left hemisphere has a particular role in the perception of emotion conveyed through meaningful speech.     

Emotion recognition and marital satisfaction in stroke

Deficits in the comprehension of facial and prosodic expressions are commonly associated with right hemisphere stroke. However, little is known regarding the impact of these disorders on social relations. We examined facial and prosodic processing, mood, and marital satisfaction in 12 right hemisphere damaged (RHD) stroke patients and nine controls. Results revealed significant impairments in the comprehension of facial expressions and prosody among RHD stroke patients. Nonparametric correlations in the RHD group showed significant associations between marital satisfaction and facial affect discrimination and matching, and nonaffective prosody discrimination. We conclude that deficits in the recognition of nonverbal expressions are associated with reduced relationship satisfaction.     

Prosopagnosia associated with a left occipitotemporal lesion

Acquired prosopagnosia is usually associated with bilateral or right-sided lesions of the occipital or temporal lobes. In rare cases of prosopagnosia after left-sided lesions in left-handed subjects, it is attributed to a reversed hemispheric specialization for face processing. This study examines the face-processing functions of a left-handed prosopagnosic patient with a left-sided lesion affecting the region of the occipital face area and possibly the fusiform face area, to contrast his deficits with those of prosopagnosic patients with right-hemispheric lesions. Similar to those patients, he has a moderately severe reduction in familiarity judgments, is impaired in processing face configuration, and shares with some of those patients a greater failure to process eye than mouth information, indicating an altered pattern of facial saliency. He has a mild reduction in the identification of exemplars of non-face objects. Unlike those patients, he has better residual familiarity on a two-alternative forced-choice task and can processing facial configuration if given more time, indicating a reduction in efficiency rather than a severe limitation. He has more difficulty accessing semantic-biographic information from names. He has trouble with facial feature imagery but not imagery for global face shape. Thus this subject's deficits represent a combination of impaired familiarity and configuration processing (normally right-sided functions in right-handed subjects), and impaired feature processing and access to semantic-biographic information (normally left-sided functions). His prosopagnosia likely reflects partially anomalous rather than reversed lateralization of hemispheric perceptual functions.     

Facial closure: interrelationship with facial discrimination, other closure tests, and subjective contour illusions

Findings from previous research have argued for the dissociation of two visual-perceptual tasks traditionally thought to be mediated by the nondominant hemisphere (i.e. perceptual closure and facial discrimination). This, primarily methodological, study examined the extent to which the facial closure measure (Mooney closure faces test) involves "closure" and/or facial discrimination. A factor analysis of six visual perceptual measures, carried out separately for left brain damaged (LBDs, n=33) and right brain damaged (RBDs, n=30) patients, resulted in two relatively independent factors (i.e. a closure factor and a facial discrimination factor), with the Mooney closure faces test loading on both. The mixed factorial structure did not aid the facial closure measure's sensitivity to right-sided brain disease. Moreover, age and education intercorrelated differently with the two factors. Results argue for the use of more discrete visual-perceptual measures when examining perceptual functioning and/or right hemisphere integrity, and imply the existence of at least two discrete cortical level visual-perceptual neural systems.     

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.     

Emotional and non-emotional facial behaviour in patients with unilateral brain damage.

Aspects of emotional facial expression (responsivity, appropriateness, intensity) were examined in brain-damaged adults with right or left hemisphere cerebrovascular lesions and in normal controls. Subjects were videotaped during experimental procedures designed to elicit emotional facial expression and non-emotional facial movement (paralysis, mobility, praxis). On tasks of emotional facial expression, patients with right hemisphere pathology were less responsive and less appropriate than patients with left hemisphere pathology or normal controls. These results corroborate other research findings that the right cerebral hemisphere is dominant for the expression of facial emotion. Both brain-damaged groups had substantial facial paralysis and impairment in muscular mobility on the hemiface contralateral to site of lesion, and the left brain-damaged group had bucco-facial apraxia. Performance measures of emotional expression and non-emotional movement were uncorrelated, suggesting a dissociation between these two systems of facial behaviour.