Can We Lose Memories of Faces? Content Specificity and Awareness in a Prosopagnosic
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Can We Lose Memories of Faces? Content Specificity and Awareness in a Prosopagnosic Nancy L. Etcoff Department of Brain and Cognitive Sciences Massachusetts Institute of Technology Neuropsychology Laboratory Massachusetts General Hospital Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/3/1/25/1755723/jocn.1991.3.1.25.pdf by guest on 18 May 2021 Roy Freeman Division of Neurology New England Deaconess Hospital Beth Israel Hospital Harvard Medical School Kyle R. Cave Department of Psychology University of California, San Diego Abstract H Prosopagnosia is a neurological syndrome in which patients nonfacial channels. The only other categories of shapes that he cannot recognize faces. Kecently it has been shown that some has marked trouble recognizing are animals and emotional prosopagnosics give evidence of “covert” recognition: they expressions, though even these impairments were not as severe show greater autonomic responses to familiar faces than to as the one for faces. Three measures (sympathetic skin re- unfamiliar ones, and respond differently to familiar faces in sponse, pupil dilation, and learning correct and incorrect learning and interference tasks. Although some patients do not names of faces) failed to show any signs of covert face recog- show covert recognition, this has usually been attributed to an nition in LH, though the measures were sensitive enough to “apperceptive” deficit that impairs perceptual analysis of the reflect autonomic reactions in LH to stimuli other than faces, input. The implication is that prosopagnosia is a deficit in access and face familiarity in normal controls. Thus prosopagnosia to, or awareness of, memories of faces: the inducing brain cannot always be attributed to a mere absence of awareness injury does not destroy the memories themselves. We present (i.e., preserved information about faces whose output is dis- a case study that challenges this view. LH suffers from proso- connected from conscious cognitive processing), to an apper- pagnosia as the result of a closed head injury. He cannot rec- ceptive deficit (i.e., preserved information about faces that ognize familiar faces or report that they are familiar, nor answer cannot be accessed due to improperly analyzed perceptual questions about the faces from memory, though he can (1) input), or to an inability to recognize complex or subtly varying recognize common objects and subtly varying shapes, (2) match shapes (i.e., loss or degradation of shape memory in general). faces while ignoring irrelevant information such as emotional We conclude that it is possible for brain injury to eliminate the expression or angle of view, (3) recognize sex, age, and like- storage of information about familiar faces and certain related ability from faces, and (4) recognize people by a number of shapes. H Prosopagnosia, a term introduced by Bodamer in 1947, patient continues to recognize familiar voices, gaits, and is a disorder of visual recognition of human faces. In the so on. It is generally believed that bilateral damage to usual case, the patient cannot recognize the faces of the medial occipitotemporal regions is necessary for this individuals known prior to the onset of illness, nor those deficit to occur and all patients whose brains have been met since. The overt deficit is absolute in that the face examined postmortem have been found to have bilateral does not elicit any sense of familiarity. Recognition of damage (Damasio, Damasio, & Van Hoesen, 1982; Da- people proceeds undisturbed via other channels, and the masio, Damasio, & Tranel, 1986). However, as with all 0 I991 Masrachusetts Institute of Technology Journal of Cognitive Neuroscience Volume 3, Number 1 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1991.3.1.25 by guest on 28 September 2021 other aspects of prosopagnosia, the neuroanatomy is the cortex of monkeys have shown small populations of neu- subject of controversy: prosopagnosics with lesions only rons sensitive to faces (e.g., Perrett, Smith, Potter, Mislin, in the right hemisphere as revealed by CT scan have Head, Milner, & Jeeves, 1984) and thus there exists the been reported (DeRenzi, 1986; Landis, Cummings, Chris- possibility that faces have a distinct and separate repre- ten, Bogen, & Imhof, 1986; Michel, Perenin, & Sieroff, sentation in the brain. 1986). The second question is one of more recent origin. In this investigation we focus on two other unresolved Within the past 5 years, several laboratories have shown questions: the extent to which prosopagnosia is a dis- that prosopagnosics give evidence of selective sensitivity order limited to the recognition of faces as opposed to to familiar faces if the tasks do not require explicit rec- a more generalized deficit in recognizing objects or ob- ognition. For example, Tranel and Damasio (1985) found jects within a category, and the extent to which it rep- that galvanic skin responses were greater to familiar than resents a disorder of awareness of recognition rather to unfamiliar faces in the prosopagnosics they tested (see than of recognition itself. also Bauer, 1984, 1986; Tranel & Damasio, 1988). Covert Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/3/1/25/1755723/jocn.1991.3.1.25.pdf by guest on 18 May 2021 The first is a basic question, for if prosopagnosics are recognition has also been demonstrated using behavioral not selectively disturbed at face recognition, why suggest measures of face matching, interference, and priming a separate disorder at all, or at least why call it pro- (e.g., Bruyer, Laterre, Seron, Feyereisen, Strypstein, Pier- sop(face)agnosia? One might argue (as some have) that rard, & Rectem, 1983; De Haan, Young, & Newcombe, faces pose a difficult perceptual problem; they are harder 1987;Young, Hellawell, & De Haan, 1988), where familiar to discriminate than most other objects in the visual and unfamiliar faces have different effects. Covert rec- world. Perhaps prosopagnosia is a very mild form of ognition has also been reported via the measurement of visual agnosia, one which disrupts only the most difficult P300 amplitude of brain potentials in a prosopaganosic visual discriminations. If this was the case, one would (Renault, Signoret, Debruille, Breton, & Bolger, 1989). predict that patients might exist for whom face recogni- These results raise several questions. Will most pro- tion was selectively disturbed but that patients should sopagnosics demonstrate these effects, suggesting that not exist for whom object recognition is disturbed in the prosopagnosia is mainly a disorder of access to conscious presence of preserved face recognition. This “mild form awareness? (See Schacter, McAndrews, & Moscovitch, of visual agnosia” argument can be refuted by the pres- 1988 for a description of various disorders of this type.) ence of case reports where object agnosias do exist in If so, how can we explain prosopagnosics who do not patients with preserved face recognition (Hecaen, Gold- demonstrate covert effects? A few such cases have been blum, Masure, & Ramier, 1974; Ferro & Santos, 1984) reported (Bauer, 1986; Newcombe, Young, & De Haan, and, to a lesser extent, by studies where face recognition 1989; Young & Ellis, 1989; Sergent & Villemure, 1989) is not fully preserved but object recognition shows far and they all have been interpreted in a similar way: that greater impairment (Albert, Reches, & Silverberg, 1975; these patients have perceptual impairments that disrupt McCarthy & Warrington, 1986; see review in Young, their ability to construct representations of faces, so that 1988). incoming information about the physical properties of On the other hand, virtually all prosopagnosics have the face are not specific or accurate enough to activate been reported to have difficulties making at least some stored face representations. In fact, the presence or ab- other within-category visual discriminations (the one sence of covert recognition in prosopagnosics has been notable exception being the patient described by De- suggested as an “index” (Newcombe et al., 1989) of Renzi, 1986). The categories posing difficulties tend to which type of prosopagnosia a patient might have: one be “natural-kind’’ categories, such as animals or foods, where the problem is mainly perceptual in nature, or but there are also reports of difficulties recognizing cars, one where the problem is mainly one of memory for coins, or other sets of similar-appearing objects (e.g., face information. Bornstein, 1963; Damasio et al., 1982). Perhaps, then, The distinction between perceptual and mnestic forms prosopagnosia reflects a more generalized disorder of of agnosia dates back to Lissauer (1890) who proposed individuating members of a visually similar class of ob- a division of the agnosias into “apperceptive” and “as- jects. Furthermore, faces vary continuously along multi- sociative” forms. In “apperceptive” agnosia there is an ple quantitative dimensions. A more refined version of impairment in visual perception beyond the level of the within-class hypothesis would be that prosopagnosia primary sensory functions (such as visual field cuts). is not specific to facelike shapes but is a difficulty in “Associative” agnosics perceive adequately but do not distinguishing objects that share the same global shape recognize what they perceive-as Teuber (1968) re- but differ quantitatively along continuous dimensions marked, there is “a normal percept stripped of meaning.” (Levine & Calvanio, 1989). Finally, of course, there