Emotional Perception and Memory in Amnesia
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Neuropsychology In the public domain 1997, Vol. ll.No.1, 104-113 Emotional Perception and Memory in Amnesia Stephan B. Hamann Larry Cahill University of California, San Diego University of California, Irvine Larry R. Squire Veterans Affairs Medical Center and University of California, San Diego The authors examined whether perception of emotional stimuli is normal in amnesia and whether emotional arousal has the same enhancing effect on memory in amnesic patients as it has in healthy controls. Forty standardized color pictures were presented while participants rated each picture according to emotional intensity (arousal) and pleasantness (valence). An immediate free-recall test was given for the pictures, followed by a yes-no recognition test. Arousal and valence ratings were highly similar among the amnesic patients and controls. Emotional arousal (regardless of valence) enhanced both recall and recognition of the pictures, and this enhancement was proportional for amnesic patients and controls. Results suggest that emotional perception and the enhancing effect of emotional arousal on memory are intact in Many studies have indicated that emotional material is emotional arousal was selectively abolished by propranolol, more memorable than neutral material (Christiansen & a p-adrenergic antagonist. Yet, participant ratings of the Loftus, 1987; Craik & Blankstein, 1975; Heuer & Reisberg, emotional arousal produced by the story were unaffected by 1990; Matlin & Stang, 1978). The primary factor underlying the drug. the effect of emotion on memory appears to be emotional Several studies of experimental animals indicate that the arousal, independent of whether the arousal is pleasant or amygdala is involved in the enhancing effects of emotion on unpleasant. In studies of nonhuman animals, emotional memory (McGaugh et al., 1993). Findings from a patient arousal has been demonstrated to affect memory through the with bilateral lesions apparently restricted to the amygdala interaction of peripheral adrenergic systems with choliner- (Cahill, Babinsky, Markowitsch, & McGaugh, 1995) are gic, opioid peptidergic, and GABAergic systems in the consistent with evidence from experimental animals. Using amygdala (McGaugh et al., 1993). The amgydala also has the same emotional memory task as in the study with the been implicated in Jear conditioning (Davis, 1994; LeDoux, p-adrenergic antagonist (Cahill et al., 1994), this patient 1993). failed to benefit from emotional arousal, suggesting that the Although emotional arousal also can benefit memory by amygdala plays a crucial role in mediating the memory its effects on cognition (e.g., increased attention, deeper facilitation effect in humans. elaborative processing), the enhanced memory associated Bradley, Green wald, Petry, and Lang (1992) examined the with physiological arousal is independent of these cognitive effect of arousal (emotional intensity) and valence (pleasant- factors and can be dissociated experimentally from them. ness) on memory in college students, systematically examin- Thus, a recent study in humans (Cahill, Prins, Weber, & ing the relative influence of each factor on memory. Stimuli McGaugh, 1994), involving memory for an illustrated story, were drawn from the Internationa] Affective Picture System demonstrated that the memory facilitation associated with (IAPS; Lang, Ohman, & Vaitl, 1988), a standardized set of color slides depicting a wide variety of naturalistic subjects Stephan B. Hamann, Department of Psychiatry, University of that spans a wide range of affective reactions. The primary California, San Diego; Larry Cahill, Center for the Neurobiology finding was that the effect of emotion on memory (both of Learning and Memory, University of California, Irvine; Larry R. recall and recognition) was mediated by arousal rather than Squire, Veterans Affairs Medical Center, San Diego, and Depart- ments of Psychiatry and Neurosciences, University of California, valence. Specifically, after the effect of emotional arousal San Diego. Stephan B. Hamann is now at the Department of had been partialed out, there was virtually no effect of Psychology, Emory University. stimulus valence (pleasantness) on memory. This study and This research was supported by the Medical Research Service of others (Lang, Bradley, & Cuthbert, 1990; Russell, 1980) the Department of Veterans Affairs, National Institute of Mental have validated the dimensional approach to measuring Health Grant MH24600, the McKnight Foundation, and the emotion (arousal and valence). We have adopted the same McDonnell-Pew Center for Cognitive Neuroscience. We thank I. dimensional approach in the current study. McGaugh for his helpful comments and N. Champagne and J. Here, we examined whether the effects of emotion on Zouzounis for research assistance. Correspondence concerning this article should be addressed to memory would be observed in patients with amnesia. Little Larry R. Squire, Department of Psychiatry (116A), Veterans Affairs is known about the effect of emotion on memory in amnesic Medical Center, 3350 La Jolla Village Drive, La Jolla, California patients or even whether the emotional reactions and emo- 92161. Electronic mail may be sent to [email protected]. tional perceptions of amnesic patients are normal (however, 104 PERCEPTION AND MEMORY IN AMNESIA 105 see Hamann et al., 1996). Reports of emotional responsivity of memory was high or low (e.g., in the control and the in the amnesic syndrome have focused almost exclusively amnesic groups, respectively). on patients with alcoholic Korsakoff s syndrome (Rapaport, The first question of interest was whether the ratings of 1961; Talland, 1967). Although these reports concur in amnesic patients for the emotional stimuli would be normal characterizing the emotional responses of patients with or abnormal. The second question was whether the effect of Korsakoffs syndrome as abnormal, they differ in their emotional arousal on memory in these patients would be descriptions of the patients. Some patients are described as normal or abnormal. Another question concerned whether having reduced reactivity to emotional stimuli (sometimes the patients with Korsakoffs syndrome would exhibit abnor- referred to as flattened or blunted affect), whereas other mal emotional reactions, as previous reports have described, reports characterize other patients as overly irritable and and whether their reactions would differ from those of other hyperarousable. Similarly, the few experimental studies of amnesic patients. This was of interest partly because patients emotional reactivity in amnesic patients with Korsakoffs with Korsakoffs syndrome sometimes have frontal lobe syndrome (Douglas & Wilkinson, 1993; Markowitsch, dysfunction along with their memory deficits, and frontal Kessler, & Denzler, 1986; Oscar-Berman, Hancock, Mild- lobe dysfunction has been linked to emotional deficits worf, Hutner, & Weber, 1990) have yielded inconsistent (Stuss, Gow, & Hetherington, 1992). Finally, the emotional results. Some researchers have found their reactions normal reactions and the effects of arousal on memory were of (Douglas & Wilkinson, 1993), whereas others have found particular interest in the case of the 2 postencephalitic them either less reactive (Markowitsch et al., 1986) or more amnesic patients with amygdala damage because of the links reactive (Oscar-Berman et al., 1990) than controls. The among amygdala, emotion, and emotional memory. interpretation of these studies is complicated because differ- ent measures and materials were used to assess reactivity Method (e.g., self-reported ratings, skin conductance response, assess- ment only of negative emotions). Participants Apart from the issue of emotional perception in amnesia is the issue of whether the effect of emotional arousal on Amnesic patients. Nine amnesic patients (6 men and 3 women) memory is normal or abnormal. Anormal effect of emotional participated in this study. Four patients had Korsakoffs syndrome. All 4 had participated in quantitative magnetic resonance imaging arousal on memory in amnesia would be consistent with two (MRI), which demonstrated reductions in the volume of the notions: First, the brain structures that mediate the effect of mammillary nuclei (for R. C., J. W., and P. N., Squire, Amaral, & emotional arousal on memory (e.g., the amygdala) modulate Press, 1990; for N. F., unpublished observations). A 5th patient (M. declarative memory (McGaugh et al., 1993). Second, these G.) sustained a bilateral media] thalamic infarction, which was modulatory brain structures are distinct from the medial confirmed by MRI. Of the remaining 4 patients, 3 had bilateral temporal lobe structures important for declarative memory reduction in the size of the hippocampal formation confirmed by (Squire & Zola-Morgan, 1991). Alternately, the effect of MRI (for P. H., Squire et al., 1990; for L. J. and H. W., unpublished emotional arousal on memory may be abnormal in amnesia observations). Patient P. H. had a 6-year history of 1- to 2-min because the perception or expression of emotion is itself attacks (of possible epileptic origin) in association with gastric symptoms and transient memory impairment. In 1989 he suffered a impaired in amnesia. series of small attacks that resulted in marked and persisting The purpose of the current study was to examine whether memory impairment. Patient L. J. became amnesic gradually emotional perception is intact or impaired in amnesia and to during 1988 and 1989 without any known precipitating