How arousal modulates memory: Disentangling the effects of attention and retention

Emotion may influence memory both by altering attention and perception during encoding and by affecting memory retention. To date, studies have focused on the enhancement of memory consolidation by arousal. However, they have failed to rule out a role for attention. To specifically link memory enhancement of arousing material to modulation of memory retention, we examined recognition of neutral and arousing words at two time points and under conditions that manipulate attention during encoding. Participants were briefly presented with an arousing or neutral word at the periphery, while fixating on a central word. Recognition of peripheral words was assessed either immediately or after 24 h. Whereas recognition of neutral words became worse over time, recognition of arousing words remained the same and was better than neutral word recognition at delay. The results indicate that arousal supports slower forgetting even when the difference in attentional resources allocated to stimuli is minimized.

[1]  S. Chaiken,et al.  The generality of the automatic attitude activation effect. , 1992, Journal of personality and social psychology.

[2]  J. D. McGaugh,et al.  Beta-adrenergic activation and memory for emotional events. , 1994, Nature.

[3]  R. Logie,et al.  Age-of-acquisition, imagery, concreteness, familiarity, and ambiguity measures for 1,944 words , 1980 .

[4]  M. Packard,et al.  Amygdala Modulation of Multiple Memory Systems: Hippocampus and Caudate-Putamen , 1998, Neurobiology of Learning and Memory.

[5]  L. Cahill,et al.  Enhanced human memory consolidation with post-learning stress: interaction with the degree of arousal at encoding. , 2003, Learning & memory.

[6]  M. Gallagher,et al.  Effect of phentolamine administration into the amygdala complex of rats on time-dependent memory processes. , 1981, Behavioral and neural biology.

[7]  M. Bradley,et al.  Remembering pictures: pleasure and arousal in memory. , 1992, Journal of experimental psychology. Learning, memory, and cognition.

[8]  Elizabeth F. Loftus,et al.  Remembering emotional events: the fate of detailed information , 1991 .

[9]  W. Balch,et al.  Dimensions of mood in mood-dependent memory. , 1999, Journal of experimental psychology. Learning, memory, and cognition.

[10]  J. P. Morgan,et al.  Design and Analysis: A Researcher's Handbook , 2005, Technometrics.

[11]  A P Shimamura,et al.  Source memory enhancement for emotional words. , 2001, Emotion.

[12]  James L. McGaugh,et al.  The amygdala and emotional memory , 1995, Nature.

[13]  L. Cahill,et al.  The Neurobiology of Emotionally Influenced Memory Implications for Understanding Traumatic Memory , 1997, Annals of the New York Academy of Sciences.

[14]  Tony W Buchanan,et al.  Enhanced memory for emotional material following stress-level cortisol treatment in humans , 2001, Psychoneuroendocrinology.

[15]  William Revelle,et al.  Individual Differences and Arousal: Implications for the Study of Mood and Memory , 1990 .

[16]  Patrik Vuilleumier,et al.  Emotional facial expressions capture attention , 2001, Neurology.

[17]  Daniel Reisberg,et al.  Remembering emotional events , 1992, Memory & cognition.

[18]  W. Revelle,et al.  Personality, Motivation and Cognitive Performance. , 1999 .

[19]  P. H. Venables,et al.  CHAPTER 1 – Mechanisms, Instrumentation, Recording Techniques, and Quantification of Responses , 1973 .

[20]  G. Keppel Design and analysis: A researcher's handbook, 3rd ed. , 1991 .

[21]  G R Loftus,et al.  Eye fixations and memory for emotional events. , 1991, Journal of experimental psychology. Learning, memory, and cognition.

[22]  Burkhart Fischer,et al.  THE ROLE OF ATTENTION IN THE PREPARATION OF VISUALLY GUIDED SACCADIC EYE MOVEMENTS IN MAN , 1987 .

[23]  J. D. McGaugh Memory--a century of consolidation. , 2000, Science.

[24]  Joseph E LeDoux,et al.  Impaired fear conditioning following unilateral temporal lobectomy in humans , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  Geoffrey R. Loftus,et al.  Some facts about “weapon focus” , 1987 .

[26]  J L McGaugh,et al.  Amygdala activity at encoding correlated with long-term, free recall of emotional information. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[27]  R. Dolan,et al.  Encoding of emotional memories depends on amygdala and hippocampus and their interactions , 2004, Nature Neuroscience.

[28]  F. Craik,et al.  Levels of Pro-cessing: A Framework for Memory Research , 1975 .

[29]  E. Walker,et al.  Action decrement and its relation to learning. , 1958 .

[30]  Terry M. Libkuman,et al.  Source of arousal and memory for detail , 1999, Memory & cognition.

[31]  R. Adolphs,et al.  The amygdala's role in long-term declarative memory for gist and detail. , 2001, Behavioral neuroscience.

[32]  Daniel Reisberg,et al.  Affect and accuracy in recall: Remembering the details of emotional events , 1992 .

[33]  S. Christianson The relationship between induced emotional arousal and amnesia. , 1984, Scandinavian journal of psychology.

[34]  B. Clifford,et al.  Effects of the Type of Incident and the Number of Perpetrators on Eyewitness Memory , 1981 .

[35]  Sven-Åke Christianson,et al.  Remembering Emotional Events: Potential Mechanisms , 1992 .

[36]  R. Dolan,et al.  Effects of Attention and Emotion on Face Processing in the Human Brain An Event-Related fMRI Study , 2001, Neuron.

[37]  J. Bohannon Flashbulb memories for the space shuttle disaster: A tale of two theories , 1988, Cognition.

[38]  SOME CONDITIONS INFLUENCING SUCCESS AT SCHOOL. , 1901, Science.

[39]  R. Dolan,et al.  Dissociable Temporal Lobe Activations during Emotional Episodic Memory Retrieval , 2000, NeuroImage.

[40]  J. Easterbrook The effect of emotion on cue utilization and the organization of behavior. , 1959, Psychological review.

[41]  Larry Cahill,et al.  Epinephrine enhancement of human memory consolidation: Interaction with arousal at encoding , 2003, Neurobiology of Learning and Memory.

[42]  A. Anderson,et al.  Lesions of the human amygdala impair enhanced perception of emotionally salient events , 2001, Nature.

[43]  J. D. McGaugh,et al.  Modulating effects of posttraining epinephrine on memory: Involvement of the amygdala noradrenergic system , 1986, Brain Research.

[44]  W. F. Prokasy,et al.  Electrodermal Activity in Psychological Research , 1973 .

[45]  K. Ochsner,et al.  Are affective events richly recollected or simply familiar? The experience and process of recognizing feelings past. , 2000, Journal of experimental psychology. General.

[46]  Scott T. Grafton,et al.  Amygdala activity related to enhanced memory for pleasant and aversive stimuli , 1999, Nature Neuroscience.

[47]  E. Phelps,et al.  Arousal-Mediated Memory Consolidation: Role of the Medial Temporal Lobe in Humans , 1998 .

[48]  C. H. Hansen,et al.  Finding the face in the crowd: an anger superiority effect. , 1988, Journal of personality and social psychology.

[49]  D. Reisberg,et al.  Vivid memories of emotional events: The accuracy of remembered minutiae , 1990, Memory & cognition.

[50]  M. S. Mayzner,et al.  Cognition And Reality , 1976 .

[51]  E. Fox,et al.  Do threatening stimuli draw or hold visual attention in subclinical anxiety? , 2001, Journal of experimental psychology. General.

[52]  John D E Gabrieli,et al.  Sex differences in the neural basis of emotional memories , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[53]  R. Dolan,et al.  An emotion-induced retrograde amnesia in humans is amygdala- and β-adrenergic-dependent , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[54]  H. Merckelbach,et al.  Differential recall of central and peripheral details of emotional slides is not a stable phenomenon , 2000, Memory.

[55]  M. Gernsbacher Resolving 20 years of inconsistent interactions between lexical familiarity and orthography, concreteness, and polysemy. , 1984, Journal of experimental psychology. General.

[56]  S. Christianson,et al.  The role of age on reactivity and memory for emotional pictures. , 1990, Scandinavian journal of psychology.

[57]  J L McGaugh,et al.  Basolateral Amygdala Is Involved in Modulating Consolidation of Memory for Classical Fear Conditioning , 1999, The Journal of Neuroscience.

[58]  R. Adolphs,et al.  Impaired emotional declarative memory following unilateral amygdala damage. , 2000, Learning & memory.

[59]  Michael J Cortese,et al.  Subjective frequency estimates for 2,938 monosyllabic words , 2001, Memory & cognition.

[60]  A. Baddeley Implications of neuropsychological evidence for theories of normal memory. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[61]  A. Öhman,et al.  Preparedness and preattentive associative learning: Electrodermal conditioning to masked stimuli. , 1995 .

[62]  S. Kaplan,et al.  Paired-associate learning as a function of arousal and interpolated interval. , 1963, Journal of experimental psychology.

[63]  D. Whitteridge Movements of the eyes R. H. S. Carpenter, Pion Ltd, London (1977), 420 pp., $27.00 , 1979, Neuroscience.

[64]  Robert D. Tarte,et al.  Memory Storage as a Function of Arousal and Time with Homogeneous and Heterogeneous Lists , 1963 .

[65]  M. Lévesque Perception , 1986, The Yale Journal of Biology and Medicine.

[66]  Karl J. Friston,et al.  Brain Mechanisms for Detecting Perceptual, Semantic, and Emotional Deviance , 2000, NeuroImage.