Double Dissociation Between Overt and Covert Face Recognition
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Double Dissociation between Overt and Covert Face Recognition Daniel Tranel, Hanna Damasio, and Antonio R. Damasio University of Iowa College of Medicine Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/7/4/425/1755262/jocn.1995.7.4.425.pdf by guest on 18 May 2021 Abstract W Some patients with face agnosia (prosopagnosia) caused by same familiar faces. Taken together, the two sets of results occipitotemporal damage produce discriminatory covert re- constitute a double dissociation: bilateral occipitotemporal sponses to the familiar faces that they fail to identify overtly. damage impairs recognition but allows SCR discrimination. For ex;miple, their average skin conductance responses (SCRs) whereas bilateral ventromedial damage causes the opposite. to familiar faces are significantly larger than average SCRs to The findings suggest that the neural systems that process the unfamiliar faces. In this study we describe the opposite disso- somatic-basedvalence of stimuli are separate from and parallel ciation in four patients with bilateral ventromedial frontal dam- to the neural systems that process the factual, nonsomatic age: Thc patients recognized the identity of familiar faces information associated with the same stimuli. H normally. yet failed to generate discriminatory SCRs to those formed consent prior to participating in these expcri- INTRODUCTION ments. All nine have normal intelligence, speech and language, and attention and orientation, and all have We and others have shown that patients with prosopag- stable, focal lesions. The neuropsychological and nosia caused by bilateral occipitotemporal lesions can neuroanatomical studies were conducted according to produce discriminatory skin conductance responses the standard protocols of the Benton Neuropsychology (SCRs) to familiar faces that are otherwise unrecognized, Laboratory and the Laboratory of Neuroimaging and a phenomenon that has been termed coverr face recog- Human Neuroanatomy (Damasio & Damasio, 1989; nition (Bauer, 1984; Bauer & Verfaellie, 1988; Tranel & Damasio & Frank, 1992; Tranel, 1995). The experiments Damasio, 1985,1988).In another series of investigations, described below were conducted when the subjects we have demonstrated that patients with bilateral ven- were in the “chronic epoch,” specifically, more than 1 tromedial frontal lobe lesions fail to produce SCRs to year after lesion onset. No additional normal control emotionally charged visual stimuli such as pictures of subjects were required for this study, because our labo- mutilation and social disaster (Damasio, Tranel, & ratory already has extensive normative data for overt and Damasio, 1991). The patients with frontal damage, how- covert face processing. ever, are not prosopagnosic: their recognition of familiar Demographic data and salient neuropsychological faces is entirely intact. characteristics of the subjects are presented in Table 1. Because many familiar faces have considerable emo- The descriptive terms for the face agnosic subjects are tional value (Tranel, Fowles, & Damasio, 1985), we pre- derived from Damasio, Tranel, and Damasio (1990). The dicted that patients with ventromedial frontal damage four ventromedial subjects had bilateral lesions involving would fail to generate discriminatory SCRs to familiar the ventral and mesial aspects of the orbital cortices, and faces, i.e., would nor discriminate faces covertly, despite the lower sector of the mesial frontal region. The five having normal face recognition. In the study described occipitotemporal subjects had bilateral damage to the below we confirm this prediction. posterior sector of the inferotemporal region, especially the inferior and mesial parts of this region, or to the METHOD ventral sector of visual association cortices. or both. Subjects The study involved nine subjects, four with ventromedial Experimental Design: Stimuli and Procedures frontal lesions and five with bilateral occipitotemporal lesions. The subjects were selected from the Division’s The experiments were designed to provide a contrast Patient Registry, and all of them provided written in- between overt and covert discrimination of familiar faces. 0 I995 Massachusetts Institute of Technology Journal of Cognitiile Neuroscience 7: 4,pp. 425-9.32 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1995.7.4.425 by guest on 29 September 2021 Table 1. Subject Characteristics Sul~ects AKe/G‘ender/Handedrzess Neu ropsychologicul Features Ventromedial 1VR-3 18 Executive function impairments M K+20 Executive function impairments F1.- I 164 Executive function impairnients I IS-1065 Executive function impairments Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/7/4/425/1755262/jocn.1995.7.4.425.pdf by guest on 18 May 2021 Pure associative prosopagnosia; visual ohject ;ignosi;i: achromatopsia; alexia Pure associative prosopagnosia;achromatopsia; topographical agnosia Pure associative prosopagnosia; vistial object agnosia; topographical agnosia Mixed associative/apperceptive prosopagnosi;i;visu;il object agnosia; alexia; optic ataxia 1’s l)-X’h 27/M/K Apperceptive prosopagnosia, visual object agnosia Ot wt-l.ciw4 Experimeizts results. The subject was asked to n;ime each bce. or to provide a specitic description of the person whose face Stimuli. Three sets of stimuli were utilized. The first, was being shown. No time limit was imposed, and suh- termed “Retro~ade-r;amily,”comprised faces of family jects were encouraged to provide whatever information members and other close acquaintances of the subject, they could about each face. drawn from the retrograde compartment. The stimulus 2. Familiarity Ratirigs. The three sets of faces were set was customized for each subject, and the number of each intermixed, in random order, with 30 iinkimiliar stimuli varied slightly from one subject to another (spe- faces (nontargets). The complete sets were then shown cific numbers are provided in the Results tables). All faces to the subject one face at a time. For cadi t’acc. the (in this and the following two sets) were shown as subject was asked to rate the degree of f;iniiliarity, The black-and-white slides, with a neutral background and no rating scale has 6 points, ranging from 1 (“definite I-iniili- features below the neckline. arity”) to 6 (“definite unfamiliarit).”), with points in Ix- The second stimulus set, termed “Retrograde-Famous,’’ tween corresponding to lesser degrees of definitude. ’I‘he comprised eight faces of famous politicians or actors. midpoint of the scale is 3.5,and ratings from 1.00 to 3.i9 ‘lhcy were chosen because all were well-known to the denote ‘bniiliarity”of some degree, while ratings of 3.5 1 subjects, and should have been easily recognized. to 6.00 denote “unfamiliarity”of some degree. (The I;h- The third set, termed “Anterograde,”comprised eight miliarity RLitirzgs experiment was conducted rrfter the hces of persons with whom the subjects had had exten- covert-level experiment described below.) sive contact with since, but not before, the onset of their condition. For example, the set included faces of psy- chologists and physicians who had worked extensively Covert-Leiiel Experiment with the subjects. The three stimulus sets (Retrograde-Family, Retrograde- Famous, and Anterograde) described above for the Fu- Procediires miliari[v Ratings experiment were presented to each 1. Ideiztity Recognition. Each set of faces was shown subject, and skin conductance was monitored. No verbal to the subject, one at a time. The three stimulus sets were or motor response was required. The two retrograde sets presented in the same order for all subjects and all were presented at the same testing session (Family first, experiments: Retrograde-Family, Retrograde-Famous, and Famous second), and the Anterograde set was presented Anterograde. We deliberately used an invariant order, to at a subsequent session. The slides were presented in allow comparisons with previous work in our laboratory. random order for each subject and set.Skin conductance Experiments were conducted across different testing was recorded from the right and left hands, using our sessions, however, and we were careful to ascertain that standard techniques and equipment (Tranel Sr Damasio. fatigue and habituation effects were not influencing the 1989, 1994). Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1995.7.4.425 by guest on 29 September 2021 Data Quantification and Analysis the ventromedial subjects on each dependent variable, in each of the three stimulus sets. Overt-I.cir1 Experiments Zdentijl$ Recognition. For each of the three stimulus RESULTS sets, the number of correct identifications was tallied. A correct identification was defined as a correct naming Overt-Level Experiments responsc, or a description that defined the individual Identity Recognition. For the two retrograde sets (Ta- being pictured in a unique manner, i.e., with charac- bles 2 and 3) and for the anterograde set (Table 4), the teristics that would distinguish that individual from all four ventromedial frontal subjects obtained Identity Rec- others ognition scores of 98.5,97.0,and 94.0%.By contrast, the five subjects with bilateral occipitotemporal lesions were Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/7/4/425/1755262/jocn.1995.7.4.425.pdf by guest on 18 May 2021 FurniliLirity Ratings. For each set, an average familiarity severely defective, obtaining respective scores of 9.0,5.2, rating was calculated for the target (T) and nontarget