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Mechanisms of Emotional Arousal and Lasting Declarative Memory F.M. Ashcroft and F.M. Gribble – K channel structure and function R EVIEW ATP 38 Ueda, K., Inagaki, N. and Seino, S. (1997) J. Biol. Chem. 272, 43 Bryan, J. and Aguilar-Bryan, L. (1997) Curr. Opin. Cell Biol. 9, 22983–22986 553–559 39 Carson, M.R., Travis, S.M. and Welsh, M.J. (1995) J. Biol. 44 Kane, C. et al. (1996) Nat. Med. 2, 1344–1347 Chem. 270, 1711–1717 45 Maassen, J.A. and Kadowaki, T. (1995) Diabetologia 4, 40 Gribble, F.M. et al. (1997) J. Physiol. 498, 87–98 375–383 41 Ericinscka, M. et al. (1992) Biochim. Biophys. Acta 1101, 46 Randle, P.J. (1993) Diabetologia 36, 269–275 273–295 47 Stirling, B. et al. (1995) Diabetologia 38, 1479–1481 42 Thomas, P.M. et al. (1995) Science 268, 425–429 48 Sakura, H. et al. (1996) Diabetologia 39, 1233–1237 Mechanisms of emotional arousal and lasting declarative memory Larry Cahill and James L. McGaugh Neuroscience is witnessing growing interest in understanding brain mechanisms of memory formation for emotionally arousing events, a development closely related to renewed interest in the concept of memory consolidation. Extensive research in animals implicates stress hormones and the amygdaloid complex as key,interacting modulators of memory consolidation for emotional events. Considerable evidence suggests that the amygdala is not a site of long-term explicit or declarative memory storage, but serves to influence memory-storage processes in other brain regions, such as the hippocampus, striatum and neocortex. Human-subject studies confirm the prediction of animal work that the amygdala is involved with the formation of enhanced declarative memory for emotionally arousing events. Trends Neurosci. (1998) 21, 294–299 ‘Selection is the very keel on which our mental ship is The evidence summarized here supports the view built. And in the case of memory its utility is obvious. that specific hormonal and brain systems activated by If we remembered everything, we should on most emotional arousal regulate long-term memory stor- − occasions be as ill off as if we remembered nothing.’ age7 9. Much evidence for this view comes from ani- (William James, 1890)1. mal studies using memory tasks that are rapidly acquired in a single learning episode and that differ in MAN WE MET RECENTLY was only a few blocks response requirements. The performance of an animal Afrom Oklahoma City’s Alfred R. Murrah building allows the inference that the memory of the animal of when the deadly bomb exploded on 19 April, 1995. the specific training situations is declarative in nature. He described that experience as ‘engraved’ in his brain, However, direct evidence for involvement of these saying, ‘I’ll have that memory forever’. Although most brain systems in declarative memory must come from of us have not had a comparable experience, we all studies involving human subjects; these studies are have conscious memories of emotionally arousing also reviewed here. experiences, long-lasting memories that are striking in Modulation of memory storage their vividness, duration and detail. Experimental studies amply demonstrate that emotionally arousing Most studies of brain mechanisms of memory focus experiences tend to be well-remembered2. on the neural events mediating memory and the Why do explicit (or ‘declarative’) memories of anatomical locus of the ‘memory trace’. Equally emotional experiences endure? Some psychological important, however, are neurobiological systems that accounts suggest that emotional events are better regulate, or modulate, long-term memory storage. remembered because they are novel, focus attention, Long-term memories are not made instantaneously: or are often rehearsed. Such hypotheses have failed they consolidate over time after learning10−12. Recent Larry Cahill and fully to account for the experimental findings2. evidence concerning memory consolidation comes James L. McGaugh Other accounts focus on emotional responses learned from many domains of investigation, including stud- − − are at the Center through Pavlovian conditioning, and much is known ies of synaptic plasticity13 15 and behavior16 19. Elegant for the about brain processes mediating the expression of demonstrations of memory consolidation in inverte- Neurobiology of fear3,4. However, explanations based solely on brate preparations indicate that memory consolidation Learning and Pavlovian conditioning of emotional responses are is evolutionarily conserved20,21. Memory and Dept likely to be insufficient because emotionally influ- Post-training treatments modulate memory storage of Psychobiology, enced memories generally involve declarative knowl- in many learning tasks. Of particular significance is University of edge and are not restricted to evocation of learned the extensive evidence that memory can be selectively California Irvine, emotional responses. Furthermore, Pavlovian con- enhanced by post-training administration of drugs Irvine, CA 92697- ditioning can be dissociated from declarative-memory and hormones. Whether memory is enhanced or 3800, USA. formation5,6. impaired by post-training treatments depends on the 294 TINS Vol. 21, No. 7, 1998 Copyright © 1998, Elsevier Science Ltd. All rights reserved. 0166 - 2236/98/$19.00 PII: S0166-2236(97)01214-9 L. Cahill and J.L. McGaugh − Emotional arousal and declarative memory R EVIEW specific experimental conditions as A Experimental modulation of memory well as the post-training treatment used8. Exogenous Long-term Training Retention drug or hormone retention event test Role of stress-released hormones injection interval in memory consolidation The fact that recently formed memories are susceptible to ex- ogenous modulatory treatments provides the opportunity for en- B Endogenous modulation of memory dogenous modulation of memory storage for emotional events. Stress Endogenous Long-term Emotional Retention hormones are a priori candidate hormone retention experience test endogenous modulators (Fig. 1). release interval Stress-hormone systems activated by emotional situations serve the immediate adaptive needs of an Fig. 1. Parallel between (A) experimental (exogenous) modulation of memory and (B) endogenous modulation of organism22. Additionally, extensive memory. Post-learning treatments are assumed to modulate memory consolidation in a manner similar to the modu- evidence suggests they influence lation normally produced by endogenous hormones released by emotional experiences. memory storage8,9,23,24. Initial stud- ies examined the effects of post-training injections of Second, they aid future responses by enhancing the adrenal medullary hormone adrenaline on mem- declarative memory of the arousing experience ory for inhibitory-avoidance training25. Adrenaline (Fig. 2). enhanced memory in a dose-dependent way, and the Role of the amygdaloid complex in memory effects were, as predicted by the consolidation modulatory mechanisms hypothesis, time-dependent: adrenaline enhanced memory only when administered shortly after train- The hypothesis that the amygdala modulates ing, that is, at the time when it would normally be declarative-memory storage is rooted in several lines released by the aversive stimulation (footshock) used of research. Early studies demonstrated that electrical in the training. Extensive research has confirmed and stimulation of the amygdaloid complex (AC) elicits extended these findings. Adrenaline has comparable behavioral arousal (the ‘orienting reflex’) and activates effects in discrimination learning and appetitively cortical EEG (Ref. 38). It is of interest for reasons dis- motivated tasks8. Adrenaline effects on memory cussed below that the cortical arousal response elicited appear to be mediated by the activation of peripheral by AC stimulation is mediated by the stria terminalis ␤-adrenergic receptors26, located on vagal afferents (ST), a major AC pathway38. Goddard’s research39 was projecting to the nucleus of the solitary tract in the brain stem27. Additionally, the effects might involve the release of glucose28. Stimuli: Animal studies imply that activation of ␤-adrenergic external/internal receptors in humans should influence long-term declarative memory formation for emotionally arous- ing events. Several recent studies now support this implication. ␤-Adrenergic antagonists block effects of Influence Interpretation memory arousal (either emotionally or physically induced) on of meaning long-term declarative memory 29–31. storage Emotional arousal also activates adrenocortical hor- mone release (cortisol in humans). The adrenocortical response is generally viewed as the ‘second wave’ of Long-term the autonomic response to an emotional event, fol- function lowing sympathetic adrenomedullary activation24. Cognitive Autonomic Most studies of adrenocortical hormones and memory emotional response stress-hormone have examined the impairing effects of high, sus- response tained doses of the hormones. However, the well- known ‘inverted-U’ relationship between dose and Short-term retention performance suggests that lower, acute function doses of corticosterone-receptor agonists should enhance memory consolidation. Several recent studies indicate that memory is enhanced by post-training Influence immediate peripheral32–34 or central35,36 (discussed later) admin- coping behaviour istration of low doses of corticosterone-receptor agon- ists. Furthermore, adrenomedullary and adrenocorti- Fig. 2. Schematic depiction of short- and long-term functions of the stress response. The sympathetic stress response serves the cal hormones on memory interact in influencing
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