The Anatomical Basis of Prosopagnosia
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J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.37.5.489 on 1 May 1974. Downloaded from Journal of Neurology, Neurosurgery, and Psychiatry, 1974, 37, 489-501 The anatomical basis of prosopagnosia J. C. MEADOWS' From the Aphasia Unit, Boston V.A. Hospital, Boston, U.S.A., and National Hospital, Queen Square, London SYNOPSIS 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. Prosopagnosia is the specific inability to recog- recently drawn attention to the occurrence of nize familiar faces. Its clinical features have been bilateral lesions in published cases that have well reviewed by previous authors-for example, come to necropsy, although they did not con- Protected by copyright. Hecaen and Angelergues (1962). It will be sider in detail the possible significance of the pointed out here only that the severely prosopa- location of these lesions. gnosic patient typically has no difficulty recogniz- In the present author's view, there is already ing everyday objects, although he may be quite good evidence concerning the localization of unable to recognize even members of his family lesions in prosopagnosia. This conclusion is unless they speak, when he immediately recog- based upon an analysis of clinical case reports nizes their voices. Some severely prosopagnosic and a re-evaluation of pathological findings in patients may recognize certain people by utilizing reported cases. It is the purpose of this paper to some specific attribute, such as a mole on the marshal this evidence and discuss possible face, unusual height, spectacles of particular underlying mechanisms. design, individual clothes, etc. However these features can be described in verbal terms, and the visual percept of faces without such features does NEUROPSYCHOLOGICAL ASPECTS not lead to recognition. The possible significance of the anatomical http://jnnp.bmj.com/ Patients with this rare symptom have poster- lesions to be described will be better understood iorly placed cerebral lesions with physical signs if consideration is first given to the normal pro- suggesting bilateral involvement in some cases cess of facial recognition and then to the neuro- but in others there is clinical evidence only of psychological features of prosopagnosia. right hemisphere disease. Visual field defects are nearly always present, but these are not sufficient FACES AS A CATEGORY It should be realized that to account for the prosopagnosia, for other recognition of faces is a most complex and on September 30, 2021 by guest. visual material is usually perceived normally. sophisticated visual achievement which is par- Unfortunately, pathological studies have been ticularly gestalt-like in nature, for most faces are few and have not led previous authors to any resistant to verbal interpretation. We can each firm conclusions on the anatomical lesions in- probably recognize more than 1,000 faces, the volved. Rondot and Tzavaras (1969), who have majority of which differ in fine detail, but we do reviewed the subject extensively, mostly from this in a manner which it is quite impossible to the neuropsychological point of view, have convey verbally. It depends on learning what are essentially visual pattern discriminations of great I Present address: The National Hospital, Queen Square, London WCIN 3BG. complexity. 489 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.37.5.489 on 1 May 1974. Downloaded from 490 J. C. Meadows There is no obvious counterpart to facial and bird watcher mentioned in the last para- recognition in other visual experience. Thus, graph who had acquired skills with other there is no other visual category within which we categories, and subsequently lost them when are required to distinguish and remember such they developed prosopagnosia, would tend to minor differences in detail by predominantly support this 'acquired' view, as does the well- non-verbalizable means. It can be argued that known observation that 'all Chinamen look certain individuals have special experience with alike' to the untravelled Westerner, but not to particular categories (the forester with trees, the the Westerner who has spent years in the horticulturalist with flowers, etc.) and in this Orient. respect it is interesting that Bornstein (1963) The cautious conclusion is thus reached that described a birdwatcher with prosopagnosia there are special characteristics about the brain's who could no longer differentiate similar birds ability to discriminate and remember faces but and a prosopagnosic farmer (Bornstein et al., these may be acquired rather than inborn. The 1969) who could no longer identify his individual same skills may not be acquired with other cows. These however are special cases. Neverthe- categories simply because there is no cultural less, the prosopagnosic patient of DeRenzi et al. pressure to acquire them. Accordingly, facial (1968) had difficulty in distinguishing fruit (an recognition becomes by far the most complex apple from a peach) and there have been some and frequently encountered example of relatively cases with inability to distinguish particular pure visual discrimination learning that occurs in chairs (Faust, 1955) or buildings (Pallis, 1955; everyday life. Considered in this way it becomes Beyn and Knyazeva, 1962; Cole and Perez Cruet, less surprising that it may be disturbed in rela- Protected by copyright. 1964). These are less striking than the prosopa- tive isolation. gnosia possibly because they are less difficult visual tasks and also because they are less purely visual (since it is easier to describe the differences PROSOPAGNOSIA AND THE AMNESIC SYNDROME in verbal terms than with faces). Perhaps the most important recent discovery in Cases such as thosejust mentioned are relevant relation to prosopagnosia is that patients with to the question of whether there are special this condition, who are unable to recognize characteristics (apart from the complexity of the familiar faces, perhaps even those of close task) about the brain's ability to distinguish faces. friends and family, may be able to discriminate Certain experimental observations suggest that and match faces normally. In other words the the brain processes information about faces in a disturbance appears to be one of memory for different way from other visual material (see for faces. To understand this better, it is helpful to example, Yin, 1970). This is borne out by the consider some of the ways in which facial everyday observation that we are strikingly recognition has been studied, together with the http://jnnp.bmj.com/ better at recognizing a face as familiar after a results that have been obtained. single encounter than we are other material-for A considerable literature has built up in example, an individual horse or a tree. However, recent years showing that the right cerebral this does not mean that skill in perception of hemisphere plays a special role in visual percep- faces is a fundamental and primitive capacity of tion and visual memory, and indeed patients the as has been some with right hemisphere lesions who are not brain, argued by authors- suffering from clinical prosopagnosia perform for example, Bodamer (1947). It may be that we on September 30, 2021 by guest. learn to distinguish faces to a degree not seen less well than those with left hemisphere lesions with other categories because facial recognition on scored tests involving facial discrimination is from the very earliest age and throughout life (DeRenzi and Spinnler, 1966; Warrington and such an essential and determining aspect of James, 1967; Benton and Van Allen, 1968; daily living. Thus, it can be argued that we might Tzavaras et al., 1970). Such tests have been of have acquired the same perceptual skill in rela- three broad types: tion to the configuration of one tree relative to 1. Those testing visual memoryfor faces-such the next, if tree configuration were as major a as recognition of photographs of well-known determinant of behaviour as is faces. The farmer public figures (Warrington and James, 1967), or J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.37.5.489 on 1 May 1974. Downloaded from The anatomical basis ofprosopagnosia 491 of previously unknown faces after an appropriate recall was not, and from subsequent reports that delay (Milner, 1968). This type oftest is the most patients with true prosopagnosia may perform closely related to the clinical symptom of pro- normally on matching tasks. This has been so in sopagnosia and was shown statistically by these three patients so far reported (Tzavaras et al., authors in unselected series ofpatients to be most 1970; Benton and Van Allen, 1972). However a impaired in right temporal lesions. (In none fourth patient reported by DeRenzi et al. (1968) of these patients was clinical prosopagnosia performed badly on matching tasks and on both present.) immediate and delayed recall, indicating that a 2. Those testing immediate recall of pre- restricted form of amnesia cannot account for viously unfamiliar faces (DeRenzi and Spinnler, all cases. 1966; Warrington and James, 1967; Milner, There are objections to considering proso- 1968). The subject might be shown a facial pagnosia as a restricted form of the amnesic photograph which is then removed, and he is syndrome. If this were so, one would expect then immediately told to pick out the face from a amnesic patients-for example, patients with display of several faces. alcoholic Korsakoff's psychosis-also to be 3. Various matching tasks, in which a facial prosopagnosic. In fact, it is very unusual for the photograph is matched with other photographs difficulty in recognizing faces that is experienced of the same face (Benton and Van Allen, 1968; by amnesic patients to compare in severity with Tzavaras et al., 1970).