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The Covert Learning of Affective Valence Does Not Require Structures in Hippocampal System Or Amygdala

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The Covert Learning of Affective Valence Does Not Require Structures in Hippocampal System Or Amygdala The Covert Learning of Affective Valence Does Not Require Structures in Hippocampal System or Amygdala Daniel Tranel and Antonio R. Damasio University of Iowa College of Medicine Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/5/1/79/1755039/jocn.1993.5.1.79.pdf by guest on 18 May 2021 Abstract Following bilateral damage to the entire medial temporal First, Boswell’s lesions guarantee that the entorhinal and peri- lobe and interconnected cortices in the anterior temporal and rhinal cortices, hippocampus, amygdala, and higher-order neo- medial frontal regions, patient Boswell developed a severe cortices in the anterior temporal region are not required to learning defect for all types and levels of Factual knowledge, support this form of covert learning. Second, this demonstra- including faces. In the experiments described here, however, tion is possible only in a patient such as Boswell, because in we demonstrate that Boswell can acquire a nonconscious bond individuals with normal or only partially impaired factual learn- between entirely new persons and the affective valence they ing, fact memory will contaminate the performance. display. The finding is important on the followng accounts. INTRODUCTION motor skills (Damasio et al., 1989). His amnesia can be summarized as follows: (1) In the anterograde compart- Patient Boswell is a 63-year-old man who has been se- ment, he has a severe defect for all types of material verely amnesic for 15 years, following herpes simplex (e.g., objects, faces, events, names) at unique and non- encephalitis. He has been investigated in our lalxmtories unique levels. Without rehearsal, new knowledge can be on numerous occasions, and descriptions of his basic retained only up to about 40 secs, beyond which it will neuroaiiatomical and neuropsychological profiles can be disappear, to all manner of observation, without a trace. found in previous publications (Damasio, Damasio, Tra- (2) In the retrograde compartment, he has a severe de- nel, Welsh, & Brandt, 1987; Damasio, Eslinger, Damasio, fect for unique material. He is limited to a few shreds of Van Hoesen, & Cornell, 1985; Damasio, Tranel, & Da- information regarding his former occupation, the fact masio, 1989). He has bilateral lesions that involve vir- that he was married and had two children, and a few tually all the principal cortical and subcortical limbic details about the town where he lived. He cannot pro- system structures (see Fig. 1). The mesial temporal re- duce any other accurate information regarding his past. gion is destroyed bikaterally, including the amygdala, en- Even in the few instances mentioned above, he is unable torhinal cortex, and hippocampus. The temporal pole to situate the facts and events temporally in his auto- (area 38) and the middle, inferior, and fourth temporal biography, or to correlate such pieces of information to nri (areas 20 and 21) are destroyed on both sides, and one another or to other temporal markers. His retrieval area 37 (in the posterior third of the same gyri) is par- of nonunique material is relatively less impaired. tially damaged on both sides. Both insular cortices are With regard to face recognition, Boswell has a severe destroyed, along with both posterior orbital cortices and defect in the retrograde compartment, and he cannot basal forebrain regions. However, the motor and pre- recognize faces of family members, long-time work as- motor cortices, basal ganglia, internal capsule, and cere- sociates, or even photographs of himself. However, we bellum are intact on both sides, as are all primary and have shown that he does demonstrate electrodermal most early sensory association cortices in occipital, tem- (skin conductance) discrimination of highly familiar faces poral, and parietal cortices. Most association cortices in from the retrograde compartment (Tranel & Damasio, the prefrontal region are intact bilaterally, including the 1987). He also produces accurate forced choice perform- entire expanse of dorsolateral frontal cortices. ances for familiar retrograde faces, and because his con- Boswell does not have perceptual defects (except for fidence ratings in these tasks were virtaally zero (i.e., he anosmia), nor does he have any language impairment. was “guessing” on every selection), we have taken the Motor function is normal, and so is the acquisition of accurate forced choice behavior, together with the elec- 0 1993 hfmuchusetts Institute of Technology Journal of Cognitive Neuroscience 5:1,pp. 79-88 (1993) Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1993.5.1.79 by guest on 25 September 2021 Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/5/1/79/1755039/jocn.1993.5.1.79.pdf by guest on 18 May 2021 Boswell Figure 1. The neuroanatomical analysis of Boswell’s lesions, based on CT and MR, was conducted according to a standard template charting technique (Damasio & Damasio, 1989), and to the new BRAINVOX technique, which performs in viuo three-dimensional brain reconstruction based on high-resolution MK slices (Damasio & Frank, 1992). The bilateral lesions have destroyed the mesial temporal region (entorhinal and perirhinal cortices, aniygdala, hippocampus), the temporal pole (area 3H), the anterior portions of the middle, inferior, and fourth temporal gyri (areas 20, 21, and anterior sector of 37), the insular region, the posterior orbital cortices, and the anterior sector of the basal forebrain. The motor and premotor cortices, however, are intact on both sides, as are all primary and early sensory association cortices (olfaction excepted). Most association cortices in the prefrontal region are also intact bilaterally, including those in the entire dorsolateral region. trodermal findings, as evidence for “covert” recognition METHODS AND RESULTS of familiar faces in the retrograde compartment. How- We tested the hypothesis that Boswell is capable of ac- ever, none of these outcomes was obtained in the antero- quiring information about new persons, provided the grade compartment. Boswell did not have discriminatory individuals are paired with a strong affective valence (the skin conductance responses to faces that he ought to operationalization of affective valence is explained be- have learned well, nor did he perform differently from low). In Experiment #1, standard “overt-level” recogni- chance in forced choice paradigms (Trdnel & Damasio, tion was tested (recognition of identity, verbal ratings of 1987). Boswell’s face learning in the anterograde com- familiarity). In Experiment #2, skin conductance and partment, which is the focus of the current set of studies, forced choice techniques were used to probe “covert” is discussed at greater length immediately below. face recognition.’ It is important to note that in these In keeping with his severe amnesia, Boswell has not experiments, the familiar faces did not have any partic- learned the faces of any of the persons he has come into ular affective value. They were faces that Boswell should contact with since the onset of his condition. He shows have learned because under normal conditions, robust no hint of recognition for the faces of physicians, psy- learning would have taken place given the abundant chologists, or caregivers, with whom he has had numer- exposure; however, the faces were not subjected to ous and extensive contacts during the past decade. any systematic manipulation involving affective valence. In However, we observed that in his daily environment (a Experiment #3, affective valences were manipulated to care facility), Boswell appeared to demonstrate a consis- determine whether this could influence face learning in tent preference relative to one of his caregivers (see Boswell, as suggested by the field observations men- Tranel & Damasio, 1990, for a preliminary report of this tioned above. Experiments #4 and #5 provided repli- observation). Specifically, there was one nursing aide to cation and follow-up whom Boswell would frequently go when he desired of Experiment #3. special treats, such as cigarettes or gum. For as long as the aide worked at this facility, he obliged Boswell’s Experiment #1: “Overt-Level”Face Learning requests, and Boswell appeared to gravitate toward this person, even if he could not overtly recognize him from Stimuli and Procedure a photograph, or address him by name. This behavior It was noted above that Boswell has not learned any new suggested that Boswell had learned some new informa- faces during the 15-year period of his amnesia, including tion vis-a-vis the aide, and the experiments we report the faces of caregivers, professionals, or other individu- here were designed to explore this phenomenon. als. To establish in systematic fashion his face learning 80 Journal of Cognitive Neuroscience Volume 5,Number 1 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1993.5.1.79 by guest on 25 September 2021 defect, the following experiments were conducted. We 2A. Skin conductance responses: Boswell’s skin selected eight faces from each of two groups: conductance was recorded, following the proce- dures we have utilized previously to measure non- 1. Professionals: physicians, psychologists, and other conscious, covert face recognition (Tranel & professionals Boswell has encountered frequently since Damasio, 1988; Tranel & Damasio, 1989). The two his illness; sets of faces were the same as in Experiment #1B. 2. Caregivers:various nursing aides and other persons Each set comprised a randomly ordered series of who live with Boswell in his care faci1ity.l The faces were 38 faces either containing the eight Professionals photographed against a white background and prepared faces or the eight Caregivers faces, mixed with non- as black-and-white slides. targets. Boswell viewed the faces but did not make Boswell’s “overt” recognition of these faces was tested any verbal response. as follows: 2B. Two-alternative forced choice: The eight Professionals and eight Caregivers faces were Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/5/1/79/1755039/jocn.1993.5.1.79.pdf by guest on 18 May 2021 1A. Identity recognition: Boswell was shown the paired with nontargets.
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