The Cognitive and Neural Mechanisms Underlying the Enhancing Effects of Emotional Memory Encoding

Abstract

Abstract: Memories for emotional information tend to be significantly enhanced in both memory accuracy and details versus neutral stimulus. These enhancing effects is influenced by emotional valence and arousal on the initial memory encoding. The regions engaged during encoding include bilateral amygdale, anterior hippocampus, parahippocampal gyrus and PFC. Amygdala-MTL system primarily support memory enhancing effects for arousing information, which reflects the automatic influence of emotion on memory and belongs to automatic processing. The processing is modulated by emotional arousal. By contrast, PFC networks recruited for the enhancing effects of encoding of negative nonarousing information. The processing for valence information belongs to controlled processing and is modulated by emotional valence.

Key words: emotional memory encoding, enhancing effect, valence, arousal, cognitive and neural mechanisms.

摘要： 相对于中性刺激,情绪信息在记忆的准确性和细节方面都会得到显著的增强,这种增强效应在编码阶段受到情绪效价和唤醒的影响。涉及到的脑区主要包括：双侧杏仁核、海马前部、海马回和前额叶皮层。杏仁核—内侧颞叶（MTL）系统支持唤醒信息的编码增强效应,反映的是情绪对记忆自动化的影响,属于自动加工,主要受情绪唤醒的调节;前额叶网络支持消极无唤醒信息的编码增强效应,对情绪信息的加工属于控制加工,主要受情绪效价的调节。

关键词: 情绪记忆的编码, 增强效应, 效价, 唤醒, 认知神经机制。

CLC Number:

B842

Wang Kejing, Kang Cheng, Wang Zhenhong, Du Lin. The Cognitive and Neural Mechanisms Underlying the Enhancing Effects of Emotional Memory Encoding[J]. Studies of Psychology and Behavior, 2013, 11(2): 282-288.

王克静, 康诚, 王振宏, 杜琳. 情绪记忆编码增强效应的认知神经机制[J]. 心理与行为研究, 2013, 11(2): 282-288.

References

1 Adolphs, R., Cahill, L., Schul, R., & Babinsky, R.(1997). Impaired declarative memory for emotional material following bilateral amygdala damage in humans. Learning & Memory, 4 , 291-300.
2 Adolphs, R., Tranel, D., & Buchanan, T. W.(2005). Amygdala damage impairs emotional memory for gist but not details of complex stimuli. Nature Neuroscience, 8 , 512-518.
3 Alvarez, R. P., Biggs, A., Chen, G., Pine, D. S., & Grillon, C.(2008). Contextual fear conditioning in humans: Cortical-hippocampal and amygdala contributions. Journal of Neuroscience, 28 , 6211-6219.
4 Cahill, L., Uncapher, M., Kilpatrick, L., Alkire, M. T., & Turner, J.(2004). Sex-related hemispheric lateralization of amygdala function in emotionally influenced memory: An FMRI investigation. Learning and Memory, 11 , 261-266.
5 Cain, M. E., Kapp, B. S. & Puryear, C. B.(2002). The contribution of the amygdala to conditioned thalamic arousal. The Journal of Neuroscience, 22 , 11026-11034.
6 Christianson, S.(1992). Emotional stress and eyewitness memory: A critical review. Psychological Bulletin, 112 , 284-309.
7 Craik, F. I., Govoni, R., Naveh-Benjamin, M. & Anderson, N. D.(1996). The effects of divided attention on encoding and retrieval processes in human memory. Journal of Experimental Psychology: General, 125 , 159-180.
8 Davidson, R. J.(1998). Anterior electrophysiological asymmetries, emotion, and depression: Conceptual and methodological conundrums. Psychophysiology, 35 , 607-614.
9 Davis, M., & Whalen, P. J.(2001). The amygdala: Vigilance and emotion. Molecular Psychiatry, 6 , 13-34.
10 Dolcos, F., Graham, R., LaBar, K., Cabeza, R.(2003). Coactivation of the amygdala and hippocampus predicts better recall for emotional than for neutral pictures. Brain & Cognition, 51 , 221-223.
11 Dolcos, F., LaBar, K. S., & Cabeza, R.(2004b). Interaction between the amygdala and the medial temporal lobe memory system predicts better memory for emotional events. Neuron, 42 , 855-863.
12 Eichenbaum, H., Yonelinas, A. P., & Ranganath, C.(2007). The medial temporal lobe and recognition memory. Annual Review of Neuroscience, 30 , 123-152.
13 Epstein, R.(2008). Parahippocampal and retrosplenial contributions to human spatial navigation. Trends in Cognitive Sciences, 12 , 388-396.
14 Fernandez, G. & Tendolkar, I.(2001). Intergrated brain activity in medial temporal and prefrontal areas predicts subsequent memory performance: Human declarative memory formation at the system level. Brain research bulletin, 55 , 1-9.
15 Ghashghaei, H. T., & Barbas, H.(2002). Pathways for emotion: Interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience, 115 , 1261-1279.
16 Guy, S. C. & Cahill, C.(1999). The role of overt rehearsal in enhanced conscious memory for emotional events. Consciousness and Cognition, 8 , 114-122.
17 Hamann, S. B.(2001). Cognitive and neural mechanisms of emotional memory. Trends in Cognitive Sciences, 5 , 394-400.
18 Hamann, S. B., Ely, T. D., Grafton, S. T., & Kilts, C. D.(1999). Amygdala activity related to enhanced memory for pleasant and aversive stimuli. Nature Neuroscience, 2 , 289-293.
19 Kensinger, E. A.(2004). Remembering emotional experiences: The contribution of valence and arousal. Reviews in the Neurosciences, 15 , 241-253.
20 Kensinger, E. A., & Corkin, S.(2004). Two routes to emotional memory: Distinct neural processes for valence and arousal . Proceedings of the National Academy of Sciences of the United States of America, 101, 3310-3315.
21 Kensinger, E. A., Garoff-Eaton, R. J., & Schacter, D. L.(2007a). Effects of emotion on memory specificity: Memory trade-offs elicited by negative visually arousing stimuli. Journal of Memory and Language, 56 , 575-591.
22 Kensinger, E. A., Garoff-Eaton, R. J., & Schacter, D. L.(2007b). How negative emotion enhances the visual specificity of a memory. Journal of Cognitive Neuroscience, 19 , 1872-1887.
23 Kilpatrick, L., & Cahill, L.(2003). Amygdala modulation of parahippocampal and frontal regions during emotionally influenced memory storage. NeuroImage, 20 , 2091-2099.
24 LaBar, K. S., & Cabeza, R.(2006). Cognitive neuroscience of emotional memory. Nature Reviews Neuroscience, 7 , 54-64.
25 Lieberman, M. D., Eisenberger, N. I., Crockett, M. J., Tom, S. M., Pfeifer, J. H., & Way, B. M.(2007). Putting feelings into words: Affect labeling disrupts amygdala activity in response to affective stimuli. Psychological Science, 18 , 421-428.
26 McGaugh, J., Introini-Collison, I., Cahill, L., Kim, M. & Liang, K.(1992). The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction . Aggleton, J. P.(Ed)(Wiley-Liss, New York), pp. 431-451
27 McGaugh, J. L.(2004). The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annual Review of Neuroscience, 27 , 1-28.
28 Mickley, K., & Kensinger, E. A.(2008). Emotional valence influences the neural corerlates associated with remembering and knowing. Cognitive, Affective and Behavioral Neuroscience, 8 , 143-152.
29 Mickley Steinmetz, K. R., & Kensinger, E. A.(2009). The effects of valence and arousal on the neural activity leading to subsequent memory. Psychophysiology, 46 , 1190-1199.
30 Murty. V. P., et al.(2010). fMRI studies of successful emotional memory encoding: A quantitative meta-analysis. Neuropsychologia, 48 , 3459-3469.
31 Murty, V. P., Sambataro, F., Das, S., Tan, H. Y., Callicott, J. H., Goldberg, T. E., et al.(2009). Age-related alterations in simple declarative memory and the effect of negative stimulus valence. Journal of Cognitive Neuroscience, 21 , 1920-1933.
32 Pape, H. C., & Pare, D.(2010). Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiological Reviews, 90 , 419-463.
33 Paz, R., Pelletier, J. G., Bauer, E. P., & Pare, D.(2006). Emotional enhancement of memory via amygdala-driven facilitation of rhinal interactions. Nature Neuroscience, 9 , 1321-1329.
34 Pessoa, L.(2009). How do emotion and motivation direct executive control? Trends in Cognitive Sciences, 13, 160-166.
35 Pitkanen, A., Savander, V., & LeDoux, J. E.(1997). Organization of intra-amygdaloid circuitries in the rat: An emerging framework for understanding functions of the amygdala. Trends in Neurosciences, 20 , 517-523.
36 Prince, S. E., Tsukiura, T., & Cabeza, R.(2007). Distinguishing the neural correlates of episodic memory encoding and semantic memory retrieval. Psychological Science, 18 , 144-151.
37 Richardson, M. P., Strange, B. A., & Dolan, R. J.(2004). Encoding of emotional memories depends on amygdala and hippocampus and their interactions. Nature Neuroscience, 7 , 278-285.
38 Ritchey, M., Dolcos, F., & Cabeza, R.(2008). Role of amygdala connectivity in the per sistence of emotional memories over time: An event-related fMRI investigation. Cerebral Cortex, 18 , 2494-2504.
39 Ritchey, M., LaBar, K. S., & Cabeza, R.(2010). Level of processing modulates the neural correlates of emotional memory formation. Journal of Cognitive Neuroscience . Advance online publication. doi:10.1162/jocn.2010.21487.
40 Roozendaal, B., McEwen, B. S., & Chattarji, S.(2009). Stress, memory and the amygdala. Nature Review Neuroscience, 10 , 423-433.
41 Rudy, J. W.(2009). Context representations, context unctions, and the parahippocampal-hippocampal system. Learning & Memory, 16 , 573-585.
42 Schwartz, G., Davidson, R., & Maer, F.(1975). Right hemisphere lateralization for emotion in the human brain: Interactions with cognition. Science, 190 , 286-288.
43 Sharot, T., & Yonelinas, A. P.(2008). Differential time-dependent effects of emotion on recollective experience and memory for contextual information. Cognition, 106 , 538-547.
44 St Jacques, P. L., Dolcos, F., & Cabeza, R.(2009). Effects of aging on functional connectivity of the amygdala for subsequent memory of negative pictures: A network analysis of functional magnetic resonance imaging data. Psychological Science, 20 , 74-84.
45 Steinmetz, K. R. M., & Kensinger, E. A.(2009). The effects of valence and arousal on the neural activity leading to subsequent memory. Psychophysiology, 46 , 1190-1199.
46 Strange, B. A., Hurlemann, R. & Dolan, R. J.(2003). An emotion-induced retrograde amnesia in humans is amygdala-and-adrenergic-dependent . Proceedings of the National Academy of Sciences of the United States of America, 100, 13626-13631.
47 Talmi, D., Anderson, A. K., Riggs, L., Caplan, J. B., & Moscovitch, M.(2008). Immediate memory consequences of the effect of emotion on attention to pictures. Learning & Memory, 15 , 172-182.
48 Van Stegeren, A. H., Roozendaal, B., Kindt, M., Wolf, O. T., & Joels, M.(2010). Interacting noradrenergic and corticosteroid systems shift human brain activation patterns during encoding. Neurobiology of Learning and Memory, 93 , 56-65.
49 Vuilleumier, P., Armony, J. L., Clarke, K., Husain, M., Driver, J. & Dolan, R. J.(2002). Neural response to emotional faces with and without awareness: event-related fMRI in a parietal patient with visual extinction and spatial neglect. Neuropsychologia, 40 , 2156-2166.
50 Whalen, P. J., Rauch, S. L., Etcoff, N. L., McInerney, S. C., Lee, M. B. & Jenike, M. A.(1998). Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. The Journal of Neuroscience, 18 , 411-418.

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