An emotion-induced retrograde amnesia in humans is amygdala- and β-adrenergic-dependent

Abstract

The influence of emotion on human memory is associated with two contradictory effects in the form of either emotion-induced enhancements or decrements in memory. In a series of experiments involving single word presentation, we show that enhanced memory for emotional words is strongly coupled to decrements in memory for items preceding the emotional stimulus, an effect that is more pronounced in women. These memory effects would appear to depend on a common neurobiological substrate, in that enhancements and decrements are reversed by propranolol, a ␤-adrenergic antagonist, and abolished by selective bilateral amygdala damage. Thus, our findings suggest that amygdaladependent ␤-adrenergic modulation of episodic encoding has costs as well as benefits. Substantial evidence indicates that enhanced memory for emotional experience engages a ␤-adrenergic system (1). ␤-Adrenergic blockade with the ␤ 1 ␤ 2 -antatgonist propranolol selectively impairs long-term human episodic memory for emotionally arousing material without affecting memory for a neutral story (2). This modulation of emotional memory by propranolol is centrally mediated, because peripheral ␤-adrenergic blockade has no such effect on emotional memory function (3). Human amygdala lesions also produce emotional memory impairment (4, 5), suggesting that this structure may represent a critical locus for propranolol's influence on emotional memory.Although emotionality is strongly associated with enhancements in memory, there is evidence for emotion-induced memory decrements (6,7). Human behavioral studies demonstrate enhanced memory for central details of an emotional event and memory suppression for peripheral details (8,9). Ecological studies show that details of an event are less likely to be remembered if followed by an emotional event (10). In experimental contexts a weak, although unreliable, effect on words presented in close proximity to potentially emotional items is reported (11). By contrast to the extensive literature on emotional enhancements in memory, nothing is known regarding the neurobiological processes accounting for emotion-induced impairments in memory.In a series of related experiments, we present psychological (Exp. 1), psychopharmacological (Exp. 2) and neuropsychological (Exp. 3) data that characterize the psychological and neurobiological properties of emotion-induced forgetting. Our first aim was to establish a behavioral index of emotion-evoked memory enhancement and impairment. In an initial behavioral memory experiment (Exp. 1), nouns were presented serially, every 3 s, in semantically related lists, and recall was tested after each list presentation. Each list, in this and subsequent experiments, contained two ''oddball'' nouns: an emotionally aversive noun (E noun) and a perceptual oddball noun (P noun), presented in a novel font (Fig. 1a). In line with previous observations (1, 6), memory for emotional items is enhanced relative to control nouns. Critically, items preceding E nouns (E-1 nouns) are recalled less well than cont...

Common regions of dorsal anterior cingulate and prefrontal–parietal cortices provide attentional control of distracters varying in emotionality and visibility

“…Previous work has found that when emotional distracters and the target stimuli are presently serially in a rapid visual stream, emotional distracters will cause significant behavioral interference ,Mitchell et al, 2006,Strange et al, 2003. However, this was not found in the current study.…”

“…Etkin et al, 2006;Haas et al, 2006). However, this was not an emotional Stroop paradigm and previous work has demonstrated that emotional distracters can cause representational interference ,Erthal et al, 2005Harris & Pashler, 2004;Mitchell et al, 2006,Okon-Singer et al, 2007,Strange et al, 2003. Of course, in many of these studies the emotional distracters have been visual images ,Erthal et al, 2005Mitchell et al, 2006; though see Harris & Pashler, 2004;Strange et al, 2003).…”

“…Indeed, while emotional distracters presented simultaneously with task relevant stimuli cause interference infrequently (Bar-Haim et al, 2007;Williams et al, 1996; though see, Erthal et al, 2005;Harris & Pashler, 2004;Okon-Singer et al, 2007). However, when emotional distracters and the target stimuli are presently serially in a rapid visual stream, interference is frequently reported ,Mitchell et al, 2006Strange et al, 2003). Two contrasting sets of predictions were made.…”

Effects of semantic relatedness on recall of stimuli preceding emotional oddballs

“…According to subjective ratings of arousal collected for this study, it also appears that semantic relationships can significantly increase arousal ratings (Figure 4a), perhaps further contributing to episodic free-recall. The finding by Strange et al (2003), demonstrating that the recall of the emotional word inhibited rather than facilitated the recall of the previous neutral word, appear to be in stark contrast to the above conclusion. However, the control words used by Strange et al (2003) all shared a semantic category, while the emotional oddball words shared only a weak semantic relationship to the preceding neutral words and had no incongruent perceptual characteristic.…”

“…Oddball studies that serially present standard stimuli and randomly insert oddballs have previously been used to demonstrate enhanced episodic free-recall for emotional oddballs, and disrupted consolidation for neutral stimuli preceding an emotional oddball (Hurlemann et al, 2005;Miu et al, 2005;Strange et al, 2003;Tulving, 1969). Increased encoding and successful remembering of the emotionally negative oddball predicts the disrupted consolidation and subsequent forgetting of the preceding neutral stimulus (Strange et al, 2003). Due to the facilitative role of semantic memory in episodic free-recall, and naturalistic accounts of increased memory for the moments preceding traumatic events (Ehlers et al, 2004(Ehlers et al, , 2002, we will examine whether a semantic relationship between an oddball and preceding stimuli can reverse disrupted consolidation and be modulated by negative emotion, resulting in greater episodic free-recall.…”