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.     

Facial recognition 1990

A review of recent studies of prosopagnosia suggests that the weight of evidence has shifted in favor of regarding it as a disability that can be produced by a right hemisphere lesion alone even though bilateral disease remains the more frequent anatomical basis. It is possible that prosopagnosia resulting from a right hemisphere lesion occurs only within the context of some atypical condition of the left hemisphere. "Types" of prosopagnosia continue to be postulated and the "identification of individuality" hypothesis continues to be advanced. Autonomic and covert recognition studies of prosopagnosic patients have described a new dimension in facial identification. Right hemisphere dominance for the discrimination of unfamiliar faces in non-aphasic patients has been confirmed but the performances of left-hemisphere damaged aphasic patients has still not been fully investigated. New developments include the study of developmental prosopagnosia and novel applications of test of facial discrimination.     

Prosopagnosia without hemianopsia after unilateral right occipitotemporal lesion

Three atypical features were noted in a patient with prosopagnosia due to a right occipital hematoma: prosopagnosia was unassociated with achromatopsia, spatial disorientation or left visual field alexia; the right visual field was normal and the left field only slightly impaired; the lesion was apparently unilateral.     

Prosopagnosia: a bihemispheric disorder.

A 54-year-old, right-handed male suffered three sequential infarcts. The first two destroyed much of the right posterior parietal area, the posterior-medial portion of the right temporal lobe and virtually the entire right occipital lobe producing left homonymous hemianopsia and left visual neglect but no prosopagnosia. A third vascular accident involved the left parieto-occipital lobe and immediately produced prosopagnosia that has persisted. The sequential correlations of lesion and symptomatology in this case demonstrate that development of persistent prosopagnosia occurred only after bilateral damage.     

Transient postoperative prosopagnosia

A 23-year-old right-handed woman developed isolated transient prosopagnosia following surgical resection of a right posterior temporal seizure focus. At 18 years of age she had developed secondarily generalized tonic-clonic seizures. Preoperative neuropsychological evaluation was normal, and neurological examination revealed only a left superior quadrant achromatopsia. MRI revealed a circumscribed lesion in the right inferolateral temporo-occipital junction. Following surgery she was agitated for 36 hours, and afterward, when her attention and orientation improved, she was unable to recognize familiar faces. She could, however, recognize familiar voices. Her prosopagnosia resolved over the next 6-7 days. This case demonstrates that isolated prosopagnosia can occur in patients with lesions restricted to the right inferior posterior temporal-anterior occipital region. The temporary nature of the prosopagnosia may result from postsurgical tissue injury, including focal cerebral edema, with compensation by ipsilateral or contralateral areas.     

Non-verbal facial and topographic visual object agnosia--a problem of familiarity in prosopagnosia and topographic disorientation

In recent years, prosopagnosia is defined as the "loss of ability to recognize the well-acquainted persons like the family members by their physiognomy." There are many reports based on this definition. However, from the viewpoint of symptomatology, there are many problems not entirely solved yet. And the mechanism of its manifestation is not clearly explained. Topographic disorientation, which often accompanies prosopagnosia, is studied even less. From the results of the postmortem examination in the literature, bilateral occipito-temporal lesions have been known to cause prosopagnosia. However, the recent radiographical examination by the computed tomography revealed that the prosopagnosia is also caused by the right occipito-temporal lesions only. We experienced a case with prosopagnosia and topographic disorientation which were considered to be caused by infarction in the territory of the right posterior cerebral artery. Detailed symptomatological, morphological and functional examinations were carried out by means of various psychological testing, X-ray computed tomography (CT), magnetic resonance imaging (MRI) and positron emission tomography (PET). The patient was a 70-year-old right-handed man who suffered from sudden visual loss on both eyes, and was admitted to our hospital after four weeks. On examination, a decrease of visual acuity and right homonymous hemianopsia were recognized. When visual acuity was recovered, he was unable to recognize the faces of his relatives and friends, with whom he has been well acquainted for many years. He also found his own house, the buildings and streets around it as entirely unfamiliar. Seven months after the onset of the disease, examination showed he had definite prosopagnosia and topographic disorientation.(ABSTRACT TRUNCATED AT 250 WORDS)     

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.     

Emotional attention in acquired prosopagnosia

The present study investigated whether emotionally expressive faces guide attention and modulate fMRI activity in fusiform gyrus in acquired prosopagnosia. Patient PS, a pure case of acquired prosopagnosia with intact right middle fusiform gyrus, performed two behavioral experiments and a functional imaging experiment to address these questions. In a visual search task involving face stimuli, PS was faster to select the target face when it was expressing fear or happiness as compared to when it was emotionally neutral. In a change detection task, PS detected significantly more changes when the changed face was fearful as compared to when it was neutral. Finally, an fMRI experiment showed enhanced activation to emotionally expressive faces and bodies in right fusiform gyrus. In addition, PS showed normal body-selective activation in right fusiform gyrus, partially overlapping the fusiform face area. Together these behavioral and neuroimaging results show that attention was preferentially allocated to emotional faces in patient PS, as observed in healthy subjects. We conclude that systems involved in the emotional guidance of attention by facial expression can function normally in acquired prosopagnosia, and can thus be dissociated from systems involved in face identification.     

Prosopagnosia without topographagnosia and object agnosia associated with a lesion confined to the right occipitotemporal region

A patient is presented who developed prosopagnosia with a recent occipitotemporal infarct in the distribution of the right posterior cerebral artery. H ve topographical agnosia or object agnosia. He regained the ability to recognize faces of familiar persons, whereas he remained unable to identify faces of persons whom he met after the of persons whom he met after the disease onset. This case demonstrate that prosopagnosia may occur as a deficit of matching a perceived face to a memory store of the face, and that the failure to recognize unfamiliar faces may be due to the inability to form memory stores of new faces. These deficits can occur in association with a lesion confined to the right occipitotemporal region.     

Ventral simultanagnosia and prosopagnosia for unfamiliar faces due to a right posterior superior temporal sulcus and angular gyrus lesion

We report a patient with ventral simultanagnosia, prosopagnosia for “unfamiliar faces” (dorsal prosopagnosia), spatial agraphia, and constructional disorder, particularly on the left spatial side, due to a lesion in the right posterior superior and middle temporal gyri and angular gyrus. The patient showed impairment of fundamental visual and visuospatial recognition, such as in object size, configuration, and horizontal point location, which probably underlay the mechanism of simultanagnosia and prosopagnosia. This case also suggests that the coexistence of simultanagnosia and prosopagnosia results from a right hemispheric insult, and damage to the temporoparietal area interrupts the incorporation of spatial information into object recognition. This disconnection of information flow, together with impaired object recognition per se, may impair the parallel processing of multiple objects, leading to object-by-object or part-by-part 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.     

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.     

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.     

Are the lesions responsible for prosopagnosia always bilateral?

To localize the lesions responsible for prosopagnosia one must first consider how recent anatomico-physiological data have modified our view of the visual system: the visual cortex has been parceled into a mosaic of visual areas, each of them processing preferentially a particular feature (form, colour, movement); there is evidence of a face area in the monkey temporal lobe, and a new model of the inferior longitudinal fasciculus has been offered. It is currently accepted that face recognition deficits are due to bilateral occipito-temporal lesions, but in view of several recent reports in which the lesions were localized on CT or MRI one may doubt that these lesions are necessarily bilateral. In some cases a right unilateral lesion seemed to be sufficient to induce prosopagnosia.     

Cerebral lateralization of face-sensitive areas in left-handers: Only the FFA does not get it right

Face perception is highly lateralized to the right hemisphere (RH) in humans, as supported originally by observations of face recognition impairment (prosopagnosia) following brain damage. Divided visual field presentations, neuroimaging and event-related potential studies have supported this view. While the latter studies are typically performed in right-handers, the few reported cases of prosopagnosia with unilateral left damage were left-handers, suggesting that handedness may shift or qualify the lateralization of face perception. We tested this hypothesis by recording the whole set of face-sensitive areas in 11 left-handers, using a face-localizer paradigm in functional magnetic resonance imaging (fMRI) (faces, cars, and their phase-scrambled versions). All face-sensitive areas identified (superior temporal sulcus, inferior occipital cortex, anterior infero-temporal cortex, amygdala) were strongly right-lateralized in left-handers, this right lateralization bias being as large as in a population of right-handers (40) tested with the same paradigm (Rossion et al., 2012). The notable exception was the so-called ‘Fusiform face area’ (FFA), an area that was slightly left lateralized in the population of left-handers. Since the left FFA is localized closely to an area sensitive to word form in the human brain (‘Visual Word Form Area’ – VWFA), the enhanced left lateralization of the FFA in left-handers may be due to a decreased competition with the representation of words. The implications for the neural basis of face perception, aetiology of brain lateralization in general, and prosopagnosia are also discussed.     

Holistic perception of the individual face is specific and necessary: Evidence from an extensive case study of acquired prosopagnosia

We present an extensive investigation (24 experiments) of a new case of prosopagnosia following right unilateral damage, GG, with the aim of addressing two classical issues: (1) Can a visual recognition impairment truly be specific to faces? (2) What is the nature of acquired prosopagnosia? We show that GG recognizes nonface objects perfectly and quickly, even when it requires fine-grained analysis to individualize these objects. He is also capable of perceiving objects and faces as integrated wholes, as indicated by normal Navon effect, 3D-figures perception and perception of Mooney and Arcimboldo face stimuli. However, the patient could not perceive individual faces holistically, showing no inversion, composite, or whole-part advantage effects for faces. We conclude that an occipito-temporal right hemisphere lesion may lead to a specific impairment of holistic perception of individual items, a function that appears critical for normal face recognition but not for object recognition.     

Loss of topographic familiarity. An environmental agnosia

Sixteen patients manifested the syndrome of loss of environmental familiarity. The syndrome is characterized by an inability to recognize familiar surroundings in spite of relatively intact verbal memory, cognition, and perception. In addition to the loss of environmental familiarity, other clinical disturbances, including central achromatopsia, prosopagnosia, palinopsia, visual hallucinations, dressing disturbances, or impaired revisualization, were present in several cases. Radiologic studies revealed that all patients had right medial temporo-occipital lesions; three had additional left-sided lesions. Clinical observations suggest that the syndrome is a class-specific agnosia similar to prosopagnosia.     

When the brain remembers, but the patient doesn’t: Converging fMRI and EEG evidence for covert recognition in a case of prosopagnosia

The role of the occipito-temporal cortex in visual awareness remains an open question and with respect to faces in particular, it is unclear to what extent the fusiform face area (FFA) may be involved in conscious identification. An answer may be gleaned from prosopagnosia, a disorder in which familiar faces are no longer recognized. This impairment has sometimes been reported to be associated with implicit processing of facial identity, although the neural substrates responsible for unconscious processing remain unknown. In this study, we addressed these issues by investigating the functional magnetic resonance imaging (fMRI) and electroencephalography (EEG) responses to familiar and unfamiliar faces in a well-known prosopagnosic patient (P.S.). Our fMRI results show that faces known prior to the onset of prosopagnosia produce an increase in activation in the lateral fusiform gyrus encompassing the FFA, as well as the right middle frontal gyrus, when compared to unknown faces. This effect is not observed with photographs of celebrities dating after the onset of prosopagnosia. Furthermore, electrophysiological responses show that previously familiar faces differ from unfamiliar ones at around 550 msec.Since covert processing of familiarity is associated with activation in FFA, this structure does not appear to be sufficient to produce awareness of identity. Furthermore, the results support the view that FFA participates in face individuation.     

Symptoms and lesion localization in visual agnosia]

There are two cortical visual processing streams, the ventral and dorsal stream. The ventral visual stream plays the major role in constructing our perceptual representation of the visual world and the objects within it. Disturbance of visual processing at any stage of the ventral stream could result in impairment of visual recognition. Thus we need systematic investigations to diagnose visual agnosia and its type. Two types of category-selective visual agnosia, prosopagnosia and landmark agnosia, are different from others in that patients could recognize a face as a face and buildings as buildings, but could not identify an individual person or building. Neuronal bases of prosopagnosia and landmark agnosia are distinct. Importance of the right fusiform gyrus for face recognition was confirmed by both clinical and neuroimaging studies. Landmark agnosia is related to lesions in the right parahippocampal gyrus. Enlarged lesions including both the right fusiform and parahippocampal gyri can result in prosopagnosia and landmark agnosia at the same time. Category non-selective visual agnosia is related to bilateral occipito-temporal lesions, which is in agreement with the results of neuroimaging studies that revealed activation of the bilateral occipito-temporal during object recognition tasks.     

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.