Face agnosia and the neural substrates of memory.

Annual Reviews www.annualreviews.org/aronline Annu. Rev. Neurosci. 1990. 13:8~109 Copyright © 1990 by Annual Reviews Inc. All rights reserved

Annu. Rev. Neurosci. 1990.13:89-109. Downloaded from www.annualreviews.org by Michigan State University Library on 08/31/13. For personal use only.

FACE AGNOSIA AND THE NEURAL SUBSTRATES OF MEMORY Antonio

R. Damasio,

Daniel

Tranel,

and Hanna Damasio

Department of Neurology, Division of Behavioral Neurology and Cognitive Neuroscience, University of Iowa College of Medicine, Iowa City, Iowa 52242 Focal damageto selective regions of the humanassociation cortices can impair the ability to recognize the identity of previously familiar faces, even whenvisual perception and intellect remain unaltered. In general, the impairment is accompaniedby an inability to learn the identity of new faces. The phenomenonhas been noted since the turn of the century (Wilbrand 1892), and is knownas prosopagnosia, or face agnosia. Its bizarre and unseemingnature lent itself to doubts that it could be caused by specific neural dysfunction, and psychodynamicinterpretations were even offered. Recently, however, face agnosia has becomethe focus of serious study (e.g. Lhermitte et al 1972, Meadows1974, Newcombe 1979, Benton 1980, Damasio et al 1982). Face agnosia, along with the varied neuropsychological disturbances that may accompany it, can now be analyzed with experimental paradigms and correlated with neuroanatomical loci of damage identified by neuroimaging methods. This affords a rare opportunity to elucidate cognitive and neural mechanisms of perception, learning, and memoryin humans. NEUROPSYCHOLOGIC FACE AGNOSIA

CHARACTERIZATION

OF

The Presentation of Face Agnosia The flavor of face agnosia can be easily captured by a brief description of one of our typical subjects. A 65-year-old womansuddenly developed an inability to recognize the faces of her husband and daughter. She could 89 01474206X/90/030142089$02.00

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DAMASIO, TRANEL & DAMASIO

not even recognize her own face in the mirror--although she knew the face she was observing must belong to her, she did not experience a sense of familiarity whenviewing it. The faces of other relatives and friends becameequally meaningless. Yet she remained fully capable of identifying all those persons from voice. About two months prior to the onset of the prosopagnosia, she had noticed somedifficulty in her perception of colors. Specifically, colors appeared "washed out" and "dirty," although she continued seeing details of shape, depth, and movementwithout any problem. She had no other history of neurological problems, and no history of psychiatric disease. Detailed evaluation upon her admission to our department revealed that her difficulties were circumscribed to the visual domainand, even there, occurred in a most selective manner. She was entirely unable to recognize a single face of any relative or friend, either in person or from photographs. Furthermore, she did not even have a hint that the faces belonged to persons with whomshe was well acquainted. She was equally impaired in the recognition of celebrities from photographs or movies. These findings are represented by the experimental data in Table 1, which come from our patient E.H. The patient was given a series of 50 faces to identify, 8 of which were well knownto her (targets). The targets were mixed, in pseudorandomorder, with 42 photographs of persons she had never encountered before (nontargets). Twoseries were administered, one in which the target faces were of relatives, friends, and herself, and a secondin which the targets were famous actors and politicians. Each face was presented on a slide, in black and white, as a full frontal pose. Features below the neckline and in the background were masked. The nontargets were selected so as to produce a group similar to the target group in terms of age range and gender ratio. Photographic charcteristics, including brightness, contrast, resolution, etc, were comparable in the target and nontarget Talfle 1 E.H.)

Identity recognition and familiarity ratings for target and nontarget faces (patient

Identity recognition (% correct)

Averagefamiliarity rating (s.d. in parentheses)

Retrograde-family experiment Target 8 Nontarget 42

0 --

6.0 (0.0) 6.0 (0.0)

Retrograde-famous experiment Target 8 Nontarget 42

0 --

6.0 (0.0) 6.0 (0.0)

N



FACE AGNOSIA

91

faces. In addition to being asked to recognize identity, she was also asked to rate, using a six-point rating scale that ranged from "l" (definite familiarity) to "6" (definite unfamiliarity), the extent to whichshe was familiar with each face. Identity recognition was at the zero level for both family and famous faces. Also, not only did she rate all of the target faces as "unfamiliar," she assigned the highest level of confidence to her ratings, i.e. she rated as "definitely unfamiliar" all eight target faces in both sets of stimuli. A parallel defect was present in the anterograde compartment, i.e. she was never able to learn the faces of persons she encounteredafter the onset of her condition, even though she could learn to recognize those individuals from their voices and other non-face cues. The profound face recognition defect of this patient occurred against a background of otherwise virtually normal neuropsychological capacities. She had normal intellect, intact speech and language, and normal memory and learning for both verbal and nonverbal material (outside the visual realm). Recognition and naming of objects were normal in the auditory and tactile modalities. (Her visual recognition and naming of non-face stimuli, although normal at first glance, showedremarkable impairments, which are discussed in the following section.) She could read normally and she could write, with normal spelling. Of particular importance, visual acuity was 20/20 in both eyes, and she performed normally on a wide range of visuopcrceptual, visuospatial, and visuoconstruction tasks. The exceptions to the intactness of basic visual perception were: (a) defect in color perception (knownas achromatopsia); and (b) small form vision scotomata in the right superior and left superior quadrants. The patient could not perceive colors in any part of the visual field and saw form always in shades of black and white. Achromatopsia frequently accompanies"pure" prosopagnosia, as a result of the contiguity of cortical regions related to color processing and to processes necessary for face recognition (Damasioet al 1989a). By itself, however,it does not contribute to prosopagnosia. The defects in this patient were caused by infarctions in ventral visual association cortices, bilaterally, in the inferior occipital/posterior temporal region (see section on Neuroanatomical Correlates below). The infarction on the right side occurred first and caused left hemiachromatopsia, as suggested by her complaints of color perception loss. The second infarct, on the left side, further impaired her ability to process color and, in combination with the first lesion, created the neuroanatomical setting for prosopagnosia. This case exemplifies a completeface recognition defect, restricted to the visual modality, and largely conforming to the classic notion of agnosia, i.e. a normal percept stripped of its meaning.For practical classification purposes we refer to this type of presentation as "pure associative" face



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agnosia. Note, however,that we do not believe perceptual and recognition/ recall processes can ever be rigidly compartmentalized. Those processes are operated in a continuum. Furthermore, additional research in the type of subject described above mayreveal subclinical, high-level integrative defects that might well be conceptualized as perceptual. There are other intriguing presentations of face agnosia. One is a partial identity recognition defect that compromisesrecognition of most or all real faces, in real time, but spares the recognition of manyor all faces presented in photographs. The problem remains restricted to the visual modality, and is "pure" in that sense. Unlike the subject in the preceding description, this type of patient has a patent and very substantial defect in visual perception. There is difficulty in perceiving all parts of a visual array simultaneously, and in generating the image of a whole entity given a part. For instance, whenshownthe drawing of a part of an airplane, the patient is unable to imagine the whole and thus fails to recognize the stimulus. The ability to assemble parts of a modelin a meaningful ensembleis also impaired. For practical classification purposes, we refer to this type of face agnosia as "partial apperceptive," although we are just as cautious about the implications of this label as we are with the label "associative" applied above. Manypatients with manifest perceptual disorders, e.g. visual disorientation, neglect, defective pattern discrimination, impaired copying ability, impaired constructional praxis, and so on, remain fully capable of recognizing familiar faces. Suchpatients, in fact, not only remain capable of recognizing identity from faces, but they also preserve the ability to recognize the meaning of facial expressions, and to make accurate judgments about gender and age based on facial information (see control subjects in Tranel et al 1988). In other words, visuoperceptual disturbance as detected by current neuropsychological probes does not necessarily cause face agnosia (Meier &French 1965, Orgass et al 1972). It appears that other components of the recognition process must be altered for agnosia to occur. In yet another presentation of face agnosia, patients have entirely normal visual perception, but their inability to recognizeidentities is not confined to the visual modality. The patients are unable to recognize identity regardless of the sensory channel used, e.g. neither viewing a face nor listening to the appropriate voice conjures up knowledgeabout the person behind both. This type we refer to as "amnesic associative," considering that it appears in the setting of amnesia. The physiopathological significance of this type of face agnosia cannot be overemphasized. It indicates that compromiseof recall for episodic level knowledgecompromisesthe recognition of face identity, which, in turn, reveals that episodic level knowledge-the knowledge of contextual detail that defines the uniqueness of

Annual Reviews www.annualreviews.org/aronline FACE AGNOSIA


entities or events- -is critical 1988, Damasioet al 1989b).

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for face learning and recognition (Damasio

Impaired Reco~lnition of Non-face Entities in Face Agnosia Early descriptions of face agnosia suggested, erroneously, that recognition of non-face stimuli, e.g. objects, animals, houses, etc, was normal. The error is not surprising, considering that patients with face agnosia are likely to complain primarily or perhaps exclusively about the problem that most disrupts their social interactions. Closer investigation, however, reveals that other recognition defects are present. Patients with face agnosia are also impaired in the visual recognition of other unique stimuli, and even of non-unique stimuli. Typical examples of the former include houses, cars, pets, and even personal effects, such as articles of clothing (Bornstein 1963, Lhermitte 1972, Damasio et al 1982, Pallis 1955). The patient described above, for instance, had pronounceddifficulties in the recognition of her clothes, her car, and her house. She never had trouble categorizing individual stimuli at the appropriate supraordinate level-i.e. she always identified faces as "faces," cars as "cars," and houses as "houses." The problem was in assigning individual identity to various exemplars. Although not as disruptive of social interaction as the face recognition disability, these other defects were not insignificant--to locate her car in a parking lot, for example, she was forced to rely upon license plate number. The meaningof the accompanyingdefects is clear. Although faces are a problemstimulus, the dysfunction that causes the face agnosia involves detecting, from visual stimuli, the identity of manycategories of entities, not just faces. Although patients with face agnosia recognize the broad category to whichvirtually any stimulus belongs, it is clear that not all stimuli can be properly categorized (Damasioet al 1982). Any such patient can decide whether a stimulus is animate or inanimate, living or man-made,e.g. decide that a dog or an elephant are "animals," that a chair is "furniture," and that flowers or a tree are "plants." At supraordinate level, recognition operates normally. Surprisingly, however, the recognition of certain particular exemplars fails at "basic object" and "subordinate levels" [to use Rosch et al’s (1976) taxonomic level nomenclature]. For instance, one our patients with "pure associative" face agnosia was unable to distinguish a cat from a tiger or lion, although she knewthat they were animals. The patient was not being asked to recognize identity, but simply to recognize a category. The existence of defects at different taxonomiclevels is of special importance, and allows for the investigation of possible factors contributing to failure or success of recognition. Current findings suggest several relevant



94


factors (Damasio1989a): (a) similarity of physical structure amongexemplars; (b) size of the class formed by exemplars with a similar structure; (c) operation of the exemplar; (d) type of sensory and motor interaction required to mapthe exemplar; (e) value of the exemplar to the perceiver; (f) acquaintance with the exemplar. Because manyof these factors are shared by entities that belong to the same conceptual categories, the recognition performance of agnosic patients maysuperficially suggest that some categories are recognized normally while others are pervasively affected, e.g. normal recognition of inanimate, man-madeobjects such as tools, contrasted with impaired recognition with animate, natural kinds such as animals or plants. Careful analysis of the data, however, reveals that there are exceptions to the rule in both the "normal" and the "impaired" categories, and that success or failure ultimately dependson constraints governing the mappingof each individual entity (Damasio1989a). Thus, the constraints related to someentities create a burden for learning and recognition at categorical level that is just as complexas the recognition of other entities at unique level. This distinction is not merely academic,but forms the basis for rejecting the notion that semantic systems are organized, cognitively and neurally, according to conceptual definitions and respecting conceptual boundaries. In short, in virtually every instance, patients with face agnosia fail to recognize an exemplar as a unique individual. Faces and other visual stimuli alike cannot conjure up pertinent information on the basis of which identity can be recovered. In addition, somestimuli fail to be recognized even if mere categorical assignment is requested. Other Aspects

of Face Processiny

As mentioned above, although patients with face agnosia are often unable to recognize the identity behind any face, they have no difficulty recognizing faces as faces. Anotheraspect of face processing that is often intact is the recognition of facial expressions. Tranel et al (1988) demonstrated experimentally that maxaypatients are entirely normal in their ability to recognize a whole array of facial expressions presented in static photographs of humanfaces. Six facial expressions were investigated: anger, fear, happiness, sadness, surprise, and disgust. For each picture on a 24item test, subjects were asked to choose from a multiple choice list the name of the expression that was being modeled in the picture. The performances of four subjects with face agnosia were compared to normals and to a brain-damaged control group (see Table 2). Three of the patients with face agnosia performed perfectly, achieving scores fully comparable to those of the controls. Only one patient, # 2, performed defectively. This result accords with the clinical observation


95

Table 2 Recognition of the meaning of facial expressions


Subject group Controls-normal (n = 20) Controls-brain damaged(n = 26) Face agnosic patients #1 #2 #3 #4

Score 20.9/24 18.0/24 17/24 a11/24 18/24 21]24

Defectiveperformance.

that patients with face agnosia generally can tell the meaningof the facial expressions as they are produced by the persons with whomthey interact. The findings also reveal that such recognition can be based on a nonmovingstimulus, i.e. a stimulus that lacks movementunfolding in real time. Other face processing abilities preserved in such patients include the assignment of gender and the estimation of age (Tranel et al. 1988). Visual Recognition of Identity from Non-face Cues Johansson (1973) has shownthat normal individuals can recognize human patterns of movement,e.g. walking, jumping, dancing, from films depicting the motion of point-light sources placed on mainjoints of an actor dressed in black, moving against a black background (a situation in which the viewer sees nothing but movementof lighted dots against a dark background). Whenthe display was shownas a static picture, observers were unable to recognize patterns of movement,or even to recognize that the point-light sources represented humanfigures. For the dynamic patterns, the seeminglydifficult recognition task can be performedin as little as 200 msec (Johansson 1976). Other investigators have used this methodto show that persons can identify gender (Kozlowski & Cutting 1977), and can even recognize unique identity (e.g. of the self or friends; Cutting Kozlowski1977), on the basis of gait information. One intriguing finding in manypatients with face agnosia is that they are able to recognize the identity of a person on the basis of non-face visual cues, such as movementand posture (Damasioet al 1982). Given circumscribed context, in which only a limited number of identity hypotheses can be entertained, such patients will correctly guess the identity of a person with a distinctive posture of the head or trunk, or with a particular gait, or with a characteristic pattern of deportment.This finding reveals the selectivity of the visual recognition defect. Uniqueidentity can

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DAMASIO,

TRANEL

& DAMASIO

still be retrieved through visual channels based on stimuli other than faces. This is important, from a physiological standpoint, because such an ability can only be explained by the existence of a multiplicity of visual representations, keyed to a single unique entity (in this case, a person). In our view (see discussion of model, below), any of those multiple representations can provide an interface to yet other representations, visual and nonvisual, related to the unique entity.


Nonconscious

Recognition

of Faces

PSYCHOLOGICAL STUDIES Most patients with severe face agnosia report a complete inability to recognize the identity of familiar faces, and they cannot decide, on an individual basis, whether a face is familiar or not. However, certain specialized probes and paradigms have been used to showthat these patients do preserve, at a nonconsciouslevel, somecapacity to discriminate familiar from unfamiliar faces. A clear demonstration of this effect was reported by Tranel & Damasio 0985, 1988), who used the electrodermal skin conductance response (SCR) to investigate covert discrimination of familiar faces. Subjects viewedsets of facial stimuli that included a mix of target (individuals with whomthe subject was well acquainted) and nontarget (individuals the subject had never seen before) faces. Each face was presented for 2 sec, at intervals of 20-25 sec. The subject was instructed to view each face carefully, but no verbal or motor response was called for. Skin conductance responses to the stimuli were measured throughout stimulus presentation. For each face, the amplitude of the largest SCRthat began within 1 to 5 sec after stimulus onset was recorded, and then the average target SCRand nontarget SCR were calculated. Relevant data are reproduced in Table 3. Despite their severe defects in familiar face recognition, four subjects generated larger and more frequent SCRsto familiar faces, as compared to unfamiliar ones. Subject A, for example, produced an average SCRof 0.934/~S to the eight target faces, which is significantly larger than her average nontarget response of 0.048 #S (p < 0.001). In another experiment, the same effect was obtained for "famous" faces. In the anterograde compartment(i.e. in the period since the onset of agnosia), where none of these subjects has shownany conscious learning of faces encounteredsince the onset of their defect, the SCRsalso revealed significant nonconscious discrimination, although the effect was smaller than for previously knownfaces. There is other evidence from the psychophysiological domainthat individuals with face agnosia can show an appreciable amount of nonconscious familiar face discrimination. Bauer (Bauer 1984, Bauer &Verfaellie 1988), for example, used a paradigm in which SCRswere measured while subjects

Annual Reviews www.annualreviews.org/aronline FACE AGNOSIA 97 Table3 Skinconductanc~ responsesfor target andnontarg¢tfaces: Retrograde-family experiment Skinconductance responses N


Subject

Frequency (in %)

Target Nontarget

Target Nontarget

A

8

42

71

12

B

8

30

75

33

C

8

42

100

36

D

14

56

100

30

Amplitude (in ktS) Target

Nontarget

0.934 (0.723) 0.170 (0.200) 1.660 (1.110) 0.528 (0.547)

0.048 (0.134) 0.039 (0.069) 0.146 (0.317) 0.011 (0.034)

viewed and listened to correct and incorrect pairs of face-name matches. In these experiments, subjects more often showed larger SCRsto the correct face-name pairs. This effect provides convergent support for the notion that patients with face agnosia can discriminate familiar faces at a nonconscious level. OTHER PARADIGMS In a study of eye movementsin two subjects with face agnosia, Rizzo et al (1987) found that the subjects scanned facial stimuli in the same manneras normal controls. For example, the patients showed the greatest numberand duration of fixations on regions of the face that contained essential facial features, e.g. the eyes, nose, mouth, chin and hairline, just as controls did. Quantitative analysis of the scanpaths also documenteda high degree of similarity between the patients and controls. The authors concluded that impaired facial recognition and learning were not associated with impaired scanning of faces. An intriguing finding reported by Rizzo et al was that scanpath properties in face agnosic subjects varied in subtle but reliable waysdepending upon whether the face being scanned was previously knownto the subject. Whenthe transition of scanpaths amongquadrants was cast in a firstorder Markovmodel transition matrix, it appeared that scanning patterns for familiar, personally meaningful faces, were markedly different from the patterns generated for unfamiliar faces. The key difference was in the predictability of the scanpaths, with previously familiar faces generating less predictable scanpaths than novel ones. Considering that the physical contours of faces activate neural structures that drive the scanpath and alter the sequential dependenceof fixations, the results were taken to mean



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DAMASIO, TRANEL & DAMAS10

that scanpaths for familiar faces in face agnosic individuals were driven by a previously acquired and still accessible internal ’°schema." Other investigators have used different experimental paradigms to demonstrate preserved "covert" familiar face processing in face agnosic subjects, de Haanet al (1987), for example, used a reaction time paradigm in which subjects had to decide whether two photographs "matched" (were of the same individual) or did not match (were of different individuals). patient with face agnosia was faster in matchingthe identities of familiar than unfamiliar faces. This effect, whichis also manifest in normalsubjects, occurred despite the patient’s completeinability to recognize face identity, or even to classify familiar faces as "familiar" or "unfamiliar" (Young de Haan 1988). In another example, Bruyer et al (1983) demonstrated that their agnosic subject could accurately classify previously familiar faces as "knownfaces," despite his inability to recognize identity. Thesebehavioral paradigms provide corroborative support for the psychophysiological and psychophysical studies described above, in the conclusion that patients with severe inability to recognize facial identity can showreliable "covert recognition" of familiar faces. NEUROANATOMICAL FACE AGNOSIA

CORRELATES

OF

Face agnosia of the "associative" type is caused by bilateral damagein inferior occipital and temporal visual association cortices, i.e. in the inferior componentof cytoarchitectonic fields 18 and 19, and part of the nearby cytoarchitectonic field 37. The superior componentof fields 18 and 19 and the inferior parietal region (field 39) are generally intact (Figure la,b). Face agnosia of the "amnesicassociative" type is also caused by bilateral damagebut in anterior temporal regions, i.e. hippocampal system structures and the surrounding higher order cortices with which the hippocampusis interconnected (Figure la,c). The posterior occipito-temporal cortices are intact. By contrast, face agnosia of the "apperceptive" type is associated with damagein right visual association cortices within the occipital and parietal regions. Based on current evidence from our laboratory, we believe there must also be damageto inferior and superior componentof fields 18 and 19 on the right, mesially and laterally, along with damageto part of fields 39 and 37 on the right (Figure la,d). The specificity of these loci of damagecan be judged by contrasting face agnosic patients with controls whohave lesions in adjoining fields but who



FACE AGNOSIA

99

Figurela Diagramof humancytoarchitectonic fields in regions whose damageis associated with face agnosia. Note that the disposition of humanvisual cortices is remarkably different from that of the monkey.The primary visual cortex (field 17 or V1) is placed entirely on the mesial brain surface. It occupies the depths and banks of the calcarine fissure. Fields 18 and 19 contain several functional regions that have been defined neurophysiologically, e.g. V2, V3. Note also the remarkablesize of the humanfields 39 and 40 in the inferior parietal lobule and of field 37 in the posterior temporal region. The label [37 +] designates the combination of fields 37, 36, and 35 in the mesial temporal region.

Figure Ib Regions of damagecorrelated with face agnosia of the "associative" type. The lesions are bilateral and are located below the plane defined by the calcarine fissure. The lesions compromisethe inferior componentof cytoarchitectonic fields 18 and 19 and part of the nearby cytoarchitectonic field 37. Note that the superior componentof fields 18 and 19 as well as the cytoarchitectonic fields in the parietal region are not involved.



100


Figurelc Distribution of damagefound in cases of face agnosia of the "amnesic associative" type. The lesions are bilateral and involve the anterior temporal re#on but not the posterior oecipitotemporal cortices. The damage compromises the hippoeampal system (entorhinal cortex, hippocampal formation, and amygdala), as well as paralimbie and neocortical fields in cytoarchitectonic fields 38, 20, 21, and 22.

Figure ld Damagefound in face agnosia of the "apperceptive" type. Note that the lesions are in the right hemisphere and that no lesion in left cortices appears necessary. Current evidence suggests that damageto both inferior and superior componentsof fields 18 and 19, both mesially and laterally, are necessary. Damageto part of fields 39 and 37, on the right, has been found in all the cases we studied.



FACE

AGNOSIA

101

do not have face agnosia. For instance, bilateral damageof visual association cortices in the superior occipital region does not cause face agnosia. Unilateral damageto parietal or to occipito-parietal association cortices does not cause face agnosia either. In fact, unilateral damageto right occipito-parietal cortices can cause a host of visuoperceptive defects and yet spare face recognition (Meier & French 1965, Orgass et al 1972). Unilateral left parietal damagecauses neither visuoperceptive defects nor face agnosia. Thus, it appears that combinedsuperior and inferior damage in right posterior association cortices is a requisite for face agnosia. Our patient J.W. # 1324 and a recent patient described by Landis et al (1988) support this view. Unilateral damageto inferior occipito-temporal cortices does not cause full-fledged prosopagnosia. Someunilateral left occipital lesions, in addition to causing alexia, also cause partial defects of facial recognition, which we have termed "deep prosopagnosia" (Damasio et al 1988). Rather than recognizing the precise target, the patients recognize someonewhose biographical characteristics are quite close in terms of gender, age, activity, and so on (e.g. recognizing Betty Grable as Marilyn Monroe). Unilateral right occipital lesions maycause slow and erratic defects in face recognition but, again, not pervasive face agnosia. In brief, face agnosia is generally correlated with bilateral lesions located either posteriorly in the inferior occipital region or anteriorly in the temporal region. However,unilateral posterior lesions, especially those located in the right hemisphereand involving cortices in both occipital and parietal regions, can cause partial defects of face recognition. The evidence indicates unequivocally that face recognition can be performed by both right and left neural networks (as Levy et al 1972 had proposed based on their study of split-brain patients). But it is also apparent that left and right structures do not contribute equally to face recognition. The right visual cortices have a definite advantage in face processing.

COGNITIVE LEARNING

AND NEURAL ASPECTS AND RECOGNITION

OF

FACE

Wehave used the profiles of neuropsychological characteristics described above, along with their anatomical correlates, to hypothesize cognitive and neural mechanismsbehind face recognition and, by extension, visual recognition. In the sections below, we discuss the status of faces as a class of visual stimuli, and the constraints imposedon their learning and recognition. Wethen outline cognitive mechanismsand neural substrates for the process of face recognition.

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The Nature of Faces as Visual

Stimuli

In the course of a lifetime, humansencounter manythousands of faces, in person and through the media. Behind each face there is a unique individual with distinctive physical and biographical characteristics. Yet, given the frequency, ease~ and eff~ciency with which we carry out facial recognition, there is little to remindus of the complexityof the task and of the burden it must pose for the brain. A numberof reasons help explain the demands of the problem. Most obvious is the sheer volume of the task. Weare required to recognize a huge number of faces. And the problem is compounded because those many different faces must be recognized at the level of unique, individual identity. Most stimuli that humansare called upon to identify need only be recognized as membersof a conceptual class, and do not require recognition as unique individuals. Wecan interact satisfactorily with the objects we manipulate daily, the vehicles we see or use for transport, or the animals we encounter in the environment, by merely recognizing the general categories to which they belong. In some instances, subcatcgorizations arc required, e.g. "jet plane," "robin," but few exemplars require unique identification (exceptions include one’s owncar, house,

or pet). Although recognition of identity from faces is just one amongseveral means of determining unique meaning, and other means (e.g. voice, gait, context) can partially or wholly support the recognition process, it is important to note that with few exceptions, th~ non-face routes are less powerful, efficacious, and specific than the face route. The presentation of a face, without any additional clues, can lead to effective and instant identity recognition, and even fairly radical alterations in viewing angle, presence or absence of appendages (e.g. hat, earrings, mustache), context, and other such factors will normally produce only small delays and increased chance for error. By contrast, recognition based on other representations of an entity requires a considerable amountof adjuvant context in order for maximalaccuracy to be achieved. These routes are also more vulnerable to perceptual distortion. Consider, for example, the difficulty imposed on recognition from voice, when attempted over the telephone. Face processing is thus a burden with rewards. Its special requirements-for instance, the need to mapfine physical details--pay off in terms of speed and accuracy, and permit a system capable of meeting the challenges described above. Faces are not only many, and different, and unique, but they are also similar. In spite of their physical differences, faces respect such strict constraints on the variation of physical structure of components and on



FACE AGNOSIA

103

the spatial arrangement of those components that they are configurationally more alike than different. Finally, there are social demands on the process of face recognition that call for both high accuracy and high speed. In short, it is difficult to imagine another domainof knowledge controlled by an equivalent collection of constraints and demands.In that sense, faces are indeed special. It must be noted, however, that certain professional activities can create somewhat similar constraints and demands, which are not shared by all humans. An example is the task of recognizing aircraft visually, or analyzing histological material under the microscope, or judging the type and quality of dog or horse specimens. The latter task was used by Diamond& Carey (1986) to illustrate the correct point that faces are both special and not special, since there are some stimuli that under particular circumstances may pose comparable problems. Face Recoynition Processes from a Coynitive Standpoint Froma cognitive standpoint, face recognition is a process of relating some face records specific to a face, to a set of somenon-face records specific to the entity behind the face. At the identity level, the process of face recognition is one of conjuring t~p meaningfor a familiar face in the form of a unique set of coactivated memoranda,i.e. recognition is subsidiary to "recall" of a pertinent set of memories.But not all levels and types of face processing are aimed at the same cognitive demands. Recognizing a facial expression amonga limited set of possible facial expressions, while of great relevance in social interactions, requires evocation of a specific but nonunique set of memoranda. In our model, recognition of identity from faces, depends on (a) the establishment of face records (records of the physical characteristics of unique face, apprehended by vision); (b) the establishment of linkages betweenface records and non-face records (non-face records inscribe other characteristics pertinent to the entity); and (c) access to (a) and (b), to simultaneousreactivation ("recall"), at conscious level, of a set of nonface records sufficient for unequivocal identification of the possessor of the face. The process described in (a) is necessary because the separation extremely similar face patterns requires detailed mappingof face features and configurational arrangements in order to render records distinctive (Damasio 1988). As we mentioned, parallel sources of information (e.g. tell-tale appendages, movement,special environmental context) do assist with disambiguation. However,the information available in the face alone is often enough, and thus there is a clear advantage to record as muchof it as possible for each individual face. In other words, even if it can be



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argued that recognizing the identity of a given person can be successfully achieved without recording or accessing all physical details of a face, a perceiver is likely to recognize more quickly and accurately if the details are indeed recorded and accessible. Incidentally, such detailed records are indeed laid downfor faces of significant individuals, or it would not be possible for normal perceivers to recall the extraordinary amountof physical structure features that they do, and to inspect these features and ensembles with their mind’s eyes. The process described in (b) is necessary because visual records of face structure do not contain information relative to other characteristics of the entity behind the face (Damasioet al 1982). It is necessary to link face records to non-face records, first during learning and later during recognition. Non-face records are both nonverbal and verbal. They include visual records such as body parts, typical attire, typical context, characteristic motion, etc and verbal information such as names, certain demographic information, and other characteristic lcxical descriptors of the entity. For face recognition, then, the critical ingredient is the partial reconstrnetion of previous experiences related to a target face, which in turn depends on the simultaneous reconstruction of key sensory and motor components of those experiences. Viewing a familiar face leads to the activation of face records learned during previous exposures to the face, e.g. shape of face components, face contour, face motion during facial expressions and face turning, scanpaths (transition of fixations) used perceive all of the above, texture, and color. In turn, based on those many sources, combined or in isolation, non-face records acquired during previous exposures and pertinently associated with the familiar face also becomeactivated. The success of recognition depends on the activation of a sufficiently comprehensiveset of non-face records and face records, in synchronous fashion. In other words, within approximately the same time window,the perceiver must not only see aspects of the face, but also have an internally recalled experience of information that pertains uniquely to that face. In cognitive terms, face agnosia can be caused by a disturbance at any point in this multicomponent process. For instance, someperceptual defects maypreclude the activation of sometypes of face records. Or the process that mediates activation of non-face records maybe defective and fail to evoke a sufficient amountof pertinent information relative to an otherwise normal percept. Or the process may generate activations that fail to reach a level commensuratewith conscious experience and thus go unattended. Such activations would not produce evocations but rather covert activity sufficient to influence behavior in someexperimental para-

Annual Reviews www.annualreviews.org/aronline FAC~A~NOS~A 105 digms but not enoughto generate conscious mental contents. In traditional psychological teminology, one might say that they do not produce true recall, or that they produceonly partial recall.


Neural Substrates

of Face Recognition

Our account of the neural substrates of facial recognition is based on the application of a systems level model of learning and memorydiscussed elsewhere (Damasio 1989b,c). In brief, the model posits: (a) that representation of the physical properties of any entity occurs at feature level, in fragmented fashion and in anatomically separate regions of early sensory cortices and motor cortices. The patterns of neural activity corresponding to different features and dimensions of entities are thus recorded in a distributed manner in the same neural ensembles engaged during perception; (b) that the integration of the varied aspects of external and internal reality, in both perception and in recall, depends on the timelocked activation of those geographically separate sites of neural activity (the modelrejects the notion of a single site, spatial integration of different representations in higl~er-order cortices); (c) that the combinatorial arrangementsthat bind features into entities, and entities into events, i.e. their spatial and temporal coincidences, are recordedin separate neural ensembles, called convergence zones; and (d) that the separate cortical regions that record featural fragments and the convergence zones that record the combinatorial binding codes that correspond to their linkage in previous perceptual or recorded experiences are interconnected by feedforward and feedback projections. This permits convergence zones to trigger and synchronize neural activity in a waythat attempts to reproduce patterns that were pertinently associated in previous experience. Convergence zones are located throughout the telencephalon in association cortices, limbic cortices, and nonlimbicsubcortical nuclei such as the basal ganglia, and form hierarchical and heterarchical networks. In general, convergence zones located near early cortices are called "local" and bind featural components of entities. Convergence zones located further downstreamin the system are called "non-local" and bind progressively more complexentities and events. Drawing on the above framework, and taking into account the lesion method data presented above, we propose the following: 1. Face records are madeup of a variety of fragmentary representations of the physical structure of faces and of processes utilized by the brain during repeated perception of such physical structures. They include unique shapes of face contour and face components, linkage codes for their spatial assembly,their spatial transformations as viewingperspectives



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DAMASIO,

TRANEL

& DAMASIO

change, and scanpaths (transition of fixations) used and modified repeated exposure. 2. Face records are bound by "local" convergence zones, located in association cortices near and directly downstreamfrom the cortices where separate face componentsor scanpaths are represented. Such convergence zonesthus subsumesets of descriptive characteristics for different faces (i.e. they represent amodally a combinatorial arrangement of characteristics), although no single convergence zone is presumedto subsumeall traits of one face. "Local" convergence zones interact with other "local" convergence zones and also with "non-local" convergence zones located downstream in the system. The latter bind events in which a specific face has participated. Whensignaled by feedforward projections, nonlocal convergence zones project back to a multiplicity of sensory cortices, visual and not, verbal and nonverbal, where the componentsof events pertinent to a face (nonface records) can be simultaneously coactivated. 3. Face records are contained in posterior visual association cortices bilaterally (in functional regions within cytoarchitectonic fields 18 and 19, and 39 and 7), but are not evenly or symmetrically distributed in those cortices. This is a consequence of the particular anatomical and physiological arrangement of the visual cortices. The processing of visual properties such as shape, texture, color, and motion dependson varied cellular channels and cortical regions within the visually related cortices and such a functional segregation imposes a separation of the corresponding face records (see Van Essen & Maunsell 1983, Livingstone & Hubel 1988, Damasio 1985). The evidence suggests persuasively that shape-related face records are probably based on inferior visual association cortices, i.e. the records and the binding local convergence zones are preferentially located in the inferior visual cortices. This is in agreementwith behavioral lesion data in both humans (see Damasio 1985) and non-human primates (Ungerleider & Mishkin 1982). There is also preliminary evidence that static records might be skewedtowardthe left sector of those cortices, whereasrecords in which shape would be recorded dynamically with transformations around vertical and anterior-posterior axes wouldbe recorded in the right sector of the system. Our findings in patients with unilateral occipital lesions speak to this point and so do studies of face processing in normals (Sergent & Bindra 1981, Ellis 1983, Gazzaniga & Smylie 1983). The mappings of linkages amongface components, as related to scanpaths over a unique face, are likely to depend upon superiorly located cortices in the right occipito-parietal region (fields 18 and 19, as well as fields 39 and perhaps 7), in keeping with the clear role of such cortices in motion detection, motion learning, and eye movementcontrol.



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4. "Non-local" convergence zones, on the basis of which event level information can be reconstituted, arc located bilaterally in temporal neocortices of fields 20, 21, 22, 35, 36, 37, in paralimbic and limbic fields 28, 38, hippocampus and amygdala, in insular cortices, and in prefrontal cortices. Recognitionof a familiar face thus starts as face perception, in multiple visual association cortices, and terminates as synchronized multimodal recall, in multiple discrete cortical regions. The process starts in early cortices and returns to early cortices, recurrently and iteratively. By holding the record to pertinent combinatorial arrangements, convergence zones at all levels, local and nonlocal, in early, intermediate, and high-order cortices, guide the process of recurrence and iteration. The testing and refinement of the account proposed here depends on further work in humans, based on cognitive experiments in subjects with small lesion probes, along with neurophysiological studies of face processing in nonhumanprimates, building on the findings of Bruce et al (1981), Perrett et al (1982), and Baylis et al (1985).

ACKNOWLEDGMENT Supported by NINDSGrant PO1 NS1 9632.

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