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 () 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 (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 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 and 2.6%for the three sets. Statistical comparisons sup- (”I)fiic~s. ported the expected differences between the groups. There were highly significant differences on the Identity Covert-I ei !el Esperiinent Recognition score in all three stimulus sets (all ps = 0.008),reflecting the accurate performance of the ven- For each stimulus set, an average skin conductance re- tromedial subjects contrasted with the severely impaired sponse magnitude was calculated for the target (‘I7 and scores of the occipitotemporal subjects. nontargct (NT) faces, following our standard procedure (Trant.1 tk Damasio, 1989,1994).Right and left hand SCRs Fnmiliari[y Rutings. As predicted, the ventromedial were averaged in all subjects (see Tranel SZ Damasio, frontal subjects produced accurate familiarity ratings in 1 994). all three stimulus sets. By contrast, none of the occipi- The Mann-Whitney LJ test was used to perform statis- totemporal subjects produced discriminatory familiarity tical comparisons of the two subject groups (Siege], ratings to target versus nontarget faces. Average ratings 1956). We compared the occipitotemporal subjects to for both targets and nontargets fell on the “unfamiliar”

Table 2. Overt Face Recognition-Retrograde-Family

FuiniliariQ Ratings N Identity Sir bjwt (Elrgets) Recognition (%) Target Nonturyd Ventromcdial frontal

EVR-3 18 12 100 1 .o 5.8 MR-42‘) 9 100 1.3 5.4

FL-11(>i 16 94 1.2 5.9 HS-1005 8 100 1 .o 5.6

98.5 1.1 5.7 (3.0) (0.2) (0.2)

Occipit (11emporal

EH-03 i 8 0 6.0 6.0 AG- 1052 14 21 4.0 5.1 DH-1,358 16 19 4.7 6.0 RB-14‘8 21 5 5.5 5.4 PSD-8’0 8 0 4.5 4.7

9.0 4.9 5.5

(10.3) (0.8) (0.5)

p-value 0.008 0,008 0.452

Tranel et al. 427

Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1995.7.4.425 by guest on 29 September 2021 Table 3. Overt Rce Recognition-Retrogr;lde-Famous

kiniiliarity Katirigs N Identi(y Sirbjecl (Targets) Recognition (%I Target Nonliirget Vcntromedi;il front;il EVK-3 I8 8 I00 1 .o 5 0 MK-I29 8 100 1.5 51 FL-I 164 8 88 1.7 57 k1S-1065 8 100 1 .o 5.8 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 97.0 1.3 5 6 (6.0) (0.4) (0.3)

Occipitoteinporal EI1-034 0 6.0 6.0 ACi-I052 13 4.4 5.0 I)H-1358 13 4.7 5.0 IW It78 0 5.2 5.0 PSD-876 0 5.0 5.I

5.2 5.1 (7.1) (0.6)

p-VdlUe 0.008 0.008 0.45 2

side of the scale (generally in the range of 5.0-5.5). ble of producing SCRs under sonie conditions, e.g., to Statistical analyses supported these observations. There physical stimuli such as a loud noise or a deep breath was a significant difference between the groups in the (see Damasio, Tranel, & Damasio, 1991; Tranel & IFaniasio, average familiarity ratings to the target faces: as expected, 1994; Tranel, 1994). The average SCR magnitudes (in pS) the ratings of the occipitotemporal subjects were higher for physical stimuli in the four subjects were EVR-3 18 = (i.e.*closer to the “unfamiliar” end of the scale) than 0.65, MR-429 = 1.50, FL-1164 = 0.94, HS-1065 = 1.54. those of the ventromedial subjects. For the nontarget In short, there is sufficient neural apparatus to producc- faces, however, the two groups were not different, as all SCRs, per se. subjects tended to rate the unfamiliar faces at the “unfa- In accordance with previous findings, the occipitotcni- miliar” end of the scale. poral subjects produced reliable discriminatory SCRs to ‘I’he overt-level experiments thus produced the ex- target faces. The effect was present for all five subjects pected outcome: the four ventromedial subjects were in the two Retrograde experiments, and for three of the nornial. whereas the five subjects with occipitotemporal four subjects in the Anterograde experiment. lesions had severely impaired face recognition in both Statistical comparisons showed that for the trrr;qr/ retrograde and anterograde compartments. faces, the occipitotemporal subjects produced larger SCRs than the ventromedial subjects in the Retrogmdc- Family (p = 0.032) and Anterograde (p = 0.029) stiniu- Covert-Level Experiment lus sets. For the nontargets, however, the two groups All four ventromedial frontal subjects failed to generate were not different. discriniinatory SCRs to target faces in any of the three We thus confirmed that ventromedial frontal subjects stimulus sets. As shown in the upper part of Table 5, the failed to generate discriminatory covert-level responses average SCRs to target versus nontarget faces are not (SCRs) to the familiar faces they so easily recognized, different in ;my of the three stimulus sets in the ven- while occipitotemporal subjects produced discriniina- tromedial subjects. It is important to note that the ab- tory covert-level responses to the familiar faces that the), sence of SCRs to familiar faces in these experiments could not recognize. Figure 1 sums up this result. c;innot be attributed to a basic defect in skin conduc- It should be noted that our data do not allow the claim tmce responding, because all of these subjects are capa- that all types of covert-level face processing are pre-

Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1995.7.4.425 by guest on 29 September 2021 Table 4. Overt Face Recognition-Anterograde

Familiarity Ratings N Iden titt, Subject (Targets) Recognition f%) Target Nonturget Ventromedial frontal EVR-3 18 8 100 1.o 5.4 MR420 8 100 1.8 5.9 FL-110-1 8 88 1.5 5.4 HS-1065 8 88 1.9 5.0 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 94.0 I .6 5.4 (6.9) (0.4) (0.4)

Occipitotemporal EH-O.?i 0 - - AG-1OiL 13 4.8 5.7 DH-1358 0 3.9 5.8 RB-14'8 0 5.4 5.3 PSD-8'0 0 5.0 4.1

2.6 4.8 5.2

(5.8) (0.6) (0.8)

0.01 4 0.443

served or defective in the occipitotemporal or ventrome- (and for the other occipitotemporal subjects). His lesions dial frontal subjects, since we utilized one index of preclude the normal activation of processing stations covert-level discrimination (SCRs). Likewise, we did not located in association cortices along the ventral occipital attempt to include all known indices of overt-level rec- and temporal regions. The existence of those processing ognition. It is conceivable that other indices of covert stations has been inferred from neuroanatomical and discrimination (e.g., ERPs, forced choice, reaction time) neurophysiologic evidence in the monkey (Distler, Bous- would not be doubly dissociable in the same manner as saoud, Desimone, Sr Ungerleider, 1993; Felleman Sr Van the SCKs, and this remains an empirical question. How- Essen, 1991; Fujita, 'Idnaka, Ito, Sr Cheng, 1992; Gross, ever, our findings allow the conclusion that there is a 1972; Kaas, 1988; Miyashita, 1993; Perrett, Mistlin, Sr double dissociation between overt face recognition and Chitty, 1987;Rockland Sr Van Hoesen, 1994;Tanaka, Saito, covert fiicc discrimination, based on indices that have Fukada, Sr Moriya, 1991; Ungerleider Sr Mishkin, 1982), been widely used to investigate these capacities. and from lesion studies in humans (Damasio Sr Damasio, 1994; Damasio, Damasio, Tranel, Sr Brandt, 1990). The processing stations are placed within the ventral compo- DISCUSSION nent of the visual association cortices, and within the As defined by Teuber, a double dissociution consists of inferotemporal cortices. Failure in the activation of these a dissociation between two performances that occurs in stations in turn precludes the recall of information perti- oppositc directions relative to two different lesion sites nently associated with the stimuli, on which recognition (Teubcr. 1955). How can we explain the double dissocia- must rely (Damasio Sr Damasio, 1994; Daniasio, Tranel, Sr tion uncovered by our study? 'Ib present our interpreta- Damasio, 1990). By contrast, there is no damage to proc- tion, wc have chosen to contrast two subjects, one from essing stations located more dorsally and laterally in the each group. (Both subjects are typical of their group; occipitotemporal region and in the occipitoparietal re- thus, tlic discussion below can be applied to all subjects gion. Nothing prevents signaling, in both forward and from both groups.) Let us first consider subject W1478, feedback modes, among the visual cortices, the parietal as reprcsentative of the bilateral occipitotemporal cases. cortices, and the dorsolateral and ventroniedial frontal Figure LA shows in schematic fashion the hypothesized regions. neural basis for the face recognition profile of RB-1478 Some of the critical signals might come from scanpatli

Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1995.7.4.425 by guest on 29 September 2021 Table 5. Covert Face Recognition-Skin Conductance Response Magnitudes (in pS)

\'entroniedial frontal

EVR-3 1 8 0.03 0.02 0.00 0.02 0.00 0.01

MK-42') 0.20 0.27 0.1 1 0.09 0.00 0.01

11,- I 164 0.08 0.10 0.04 0.03 0.02 0.0-

I IS- I005 0.28 0.23 0.20 0.18 0.14 0.I' 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 0 15 0 16 0 09 0 08 0 o+ 0 0- (0 11) (0 12) (0 09) (0 07) (0 0') (0 OX)

( )ccipitoteniporal

El 1-034 0.93 0.05 0.73 0.01 - -

MI-I052 0.53 0.01 0.12 0.00 0.29 0.00

l)Il-l358 1.34 0.17 1.54 0.04 1.18 0.0-1 KB-14'8 0.29 0.01 0.18 0.03 0.I9 0.03 1's I 1-870 0.17 0.04 0.06 0.02 0.01 0.01

0.65 0.06 0.5:, 0.02 0.t2 0.02 (0.48) (0.07) (0.63) (0.02) (0.52) (0.02)

/,-\.;rlue 0.032 0.095 0.095 0,143 0.029 0.243

processing of faces, which tias been shown to be f;unil- iar-face specific (Rizzo, Hurtig, & Damasio, 1987).and LISC' a parietal route. Or they might come from structiir;iI kic~

50 features and be routed via temporal cortices to tlorsolat- era1 frontal structures. In either case, there are patent neuroanatomical circuits (see Goldman-Rakic, 1988; Wil- 40 son, O Scalaidlie, & Goldnian-Rakic, 1993) to support sigiialiiig from posterior visual association cortices to ln 0 frontal cortices, including those in the ventromedial re- .30 I) E gion. The latter would, in turn, signal to intact ;iutononiic ((1 2. control nuclei, which would then trigger the discrimina- ae .20 m tory electrodermal skin condiict;ince response (Fig. 2). e (For a more detailed discussion of the anatomy of this -ln chain of activation, see Ikimasio, Tranel, SZ Dani;isio. .10 1990.) Now consider the case of ventromcdial frontal subject HS-1065 (and the other ventromedial subjects; see Fig. 2H). Since the entire occipitotcniporal and occipitop:iric= I OCClpllO- vemro- occip11o- ven1ro- iemporal medial temporal msdlal tal regions ;ire intact, recall of information pertinent to visual inputs occurs normally, c.g.,seeing a face activate5 the processing stations that were damaged in the pre- Figure 1. 'l'lic rlorrbli~dissoc'itrlioii hetwc.cn overt and covert face rccognition is ilcpictcd by the gr.iph showing the ~ive~igeIdentity vious case, thus allowing for accurate identification of 1lcxx)gnition scores (left side of figure) and SCR nragnitudes (right the face. However, signals aimed at frontal cortices. re- hide 01 ligiirc) lor the four ventromedial frontal and tive occipitoteni- gardless of the route they may take, ventrally or dorsally, por~lwbjccts. ~ivcr.igeclxross both retrograde arid ;interogr.icle can no longer activate the destroyed ventronietlial re- \timulux sets. For orwt recognition. iiidcxcd by Identity Recognition. gion (Barbas, 1993; McGuire, Hates, & Goldman-R;ikic, thc occil'itotenil'or.il whjects are severely impaired. whereas the \,cntroniccli:il suhjccts arc normal. The revcrsc outconic obtains for 1991; Pandya, Seltzer, & Barbas, 1988; Seltzer SZ I?anclya. thc cowi~/index (S(:Ks). 1989; Wilson, O Scalaidlie, & Goldnian-Rakic, 1993). I'li~'

Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1995.7.4.425 by guest on 29 September 2021 namely those in the ventromedial region. On the con- A trary, generating innately set emotional responses to unconditioned stimuli is still possible and probably util- izes the intact amygdala and hypothalamus. As noted earlier, we have shown that subjects with ventromedial damage fail to respond autonomically to emotionally charged stimuli such as social disasters. We interpreted this failure to reflect an inability to evoke "somatic markers" that would normally accompany the processing of such socially charged stimuli, i.e.,the feel- ing of bodily states generated by learned emotional re- sponses (Damasio, Tranel, & Damasio, 1991). That the 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 Occipito-Temporal damage ventromedial subjects also fail to respond to familiar faces is consistent with the somatic marker hypothesis. In both situations the subjects fail to generate a "secon- dary emotion" to a stimulus whose value, negative or positive, they have learned (cf. Damasio, 1994). The findings suggest that the neural systems that proc- ess the somatic-based valence of stimuli (their emotional significance) are separate from and parallel to those that process the factual, nonsomatic information associated with those same stimuli.

Acknowledgment This research was supported by NINDS Program Project Grant NS 19632 and The Mathers Foundation.

Reprint requests should be sent to Dr. Daniel Tranel, Depart- ment of Neurology, University of Iowa Hospitals and Clinics, Figure 2. I)iagmii of possible routes of neural activation in sub- Iowa City, LA 52242. jects with occipitotemponl damage (A) or ventromcdial frontal dam- age (B). (A).The damage (cross-hatch) precludes activation (by faces) 01 ventral occipital and temporal association cortices. I)orsal cortices L tot operate, however, allowing signals to reach ventrome- REFERENCES dial front.il cortices and, in turn, activate :iiitonornic control nuclei such as ilir ;imygdal;i. (B). Faces can he processed normally in vcn- Barbas. H. ( 1993).Organization of cortical afferent input to tral occipilal and temporal association cortices. Signals aimed ;it orbitofrontal areas in the rliesus monkey. Neuroscieizce, frontal cortices. however, can no longer activate the damaged VCII- 56, 841-864. tromedi.tl lrontd cortices (cross-hatch). thus blocking activition of Rauer, R. M. (1984). Autonomic recognition of names and autonomic control nuclei such as the amygdala. The patent connec- Faces in prosopagno A neuropsychological application tion (grq ;irrow) between occipital ;issociation cortices and :iuto- of the Guilty Knowledge Test. Neurr,ps)Icholf)~i~~,22, 457- nomic cltcctors such ;IS the aniygdala would he the preferred route 469. for basic. 3tartle stimuli. Given our findings. however, this route ;ipI'ar- Bauer, R. M., Sr Verfaellie. M. (1988). Electrodermal discrimina- cntly is ,MJ/ iised for autonomic responses to conditioned stimuli tion of familiar but not tinfamiliar kices in prosopagnosia. such as t:tniiliar faces. Bruit1 und Cognition. 8,240-252. Dmiasio, A. K. (1 994). Llescartes' error: Ewzotion, rey'~isoriutid the human Druiii. New York: Grosset/Putnam. Damasio. A. R., 81 IYamasio, H. (1994). Cortical systems for re- triggering of central autonomic control nuclei from the trieval of concrete knowledge: The convergence zone ventromedial frontal cortices would be precluded, and framework. In C. Koch (Ed.), Large-scule rieiironal tlxo- electroclcrmal skin conductance responses would not ries of the 6ruin (pp. 61-74), Cambridge, MA: MIT Press. occur in response to the types of stimuli used in these Damasio. A. R., Damasio, H., Tranel, D., Sr Brandt,J. t? (1 990). The neural regionalization of knowledge access: Prelimi- experiments. nary evidence. Qicuwtitutizv Biology, 55, 1039- 1047. Sincc both the amygdala and the hypothalamus are Damasio. A. K., Tranel, I)., & Damasio, H. (19%)).Face agnosia intact in the ventromedial frontal subjects, and since all and the neural substrates of memory. Aizniial Reriieui of known routes leading to them are patent with the sole Neuroscience, 1.1. 89- 109. exception of the route that utilizes ventromedial frontal Ihmasio. A. R., Tranel. I)., Sr Damasio, H. (1991). Somatic mark- ers and the guidance of behavior: Theory and preliminary station%.this finding suggests that, at least in part, gener- testing. In H. S. Levin, H. M. Eisenberg. 8I A. L. Benton ating responses learned in connection with complex (Eds.), Frontal l06e function and dysfunction (pp. 2 17- visual stirnuli requires the agency of prefrontal cortices, 229). New York: Oxford University Press.

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