Retrieval of emotional memories.

Long-term memories are influenced by the emotion experienced during learning as well as by the emotion experienced during memory retrieval. The present article reviews the literature addressing the effects of emotion on retrieval, focusing on the cognitive and neurological mechanisms that have been revealed. The reviewed research suggests that the amygdala, in combination with the hippocampus and prefrontal cortex, plays an important role in the retrieval of memories for emotional events. The neural regions necessary for online emotional processing also influence emotional memory retrieval, perhaps through the reexperience of emotion during the retrieval process.

[1]  J. Price,et al.  The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. , 2000, Cerebral cortex.

[2]  Michael D. Rugg,et al.  Electrophysiological Correlates of the Retrieval of Emotional and Non-emotional Context , 2001, Journal of Cognitive Neuroscience.

[3]  Z. Segal,et al.  Cognitive reactivity and vulnerability: empirical evaluation of construct activation and cognitive diatheses in unipolar depression. , 2005, Clinical psychology review.

[4]  C. Brewin Understanding cognitive behaviour therapy: A retrieval competition account. , 2006, Behaviour research and therapy.

[5]  E. Tulving Memory and consciousness. , 1985 .

[6]  M. Guha Memory from A to Z: Keywords, Concepts and Beyond , 2003 .

[7]  R. Adolphs,et al.  A Role for Somatosensory Cortices in the Visual Recognition of Emotion as Revealed by Three-Dimensional Lesion Mapping , 2000, The Journal of Neuroscience.

[8]  P. Kendall,et al.  Self-referent speech and psychopathology: The balance of positive and negative thinking , 1989, Cognitive Therapy and Research.

[9]  A. P. R Smith,et al.  fMRI correlates of the episodic retrieval of emotional contexts , 2004, NeuroImage.

[10]  R. J Dolan,et al.  Common and distinct neural responses during direct and incidental processing of multiple facial emotions , 2003, NeuroImage.

[11]  A K Anderson,et al.  Contribution of the anteromedial temporal lobes to the evaluation of facial emotion. , 2000, Neuropsychology.

[12]  M. Bouton Context, time, and memory retrieval in the interference paradigms of Pavlovian learning. , 1993, Psychological bulletin.

[13]  Joseph E LeDoux,et al.  Human Amygdala Activation during Conditioned Fear Acquisition and Extinction: a Mixed-Trial fMRI Study , 1998, Neuron.

[14]  Reconsolidation after remembering an odor-reward association requires NMDA receptors. , 2005, Learning & memory.

[15]  Michael Davis,et al.  Extinction of fear-potentiated startle: blockade by infusion of an NMDA antagonist into the amygdala , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  Daniel L. Schacter,et al.  See Blockindiscussions, Blockinstats, Blockinand Blockinauthor Blockinprofiles Blockinfor Blockinthis Blockinpublication Retrieving Blockinaccurate Blockinand Blockindistorted Blockinmemories: Neuroimaging Blockinevidence Blockinfor Blockineffects Blockinof Blockinemotion , 2022 .

[17]  L. Obler,et al.  Right hemisphere emotional perception: evidence across multiple channels. , 1998, Neuropsychology.

[18]  F. Bartlett,et al.  Remembering: A Study in Experimental and Social Psychology , 1932 .

[19]  A. Grace,et al.  The Prefrontal Cortex Regulates Lateral Amygdala Neuronal Plasticity and Responses to Previously Conditioned Stimuli , 2003, The Journal of Neuroscience.

[20]  Elliot A. Stein,et al.  Amygdala and hippocampal activity during acquisition and extinction of human fear conditioning , 2007 .

[21]  J. Bremner,et al.  Are the neural substrates of memory the final common pathway in posttraumatic stress disorder (PTSD)? , 2002, Journal of affective disorders.

[22]  S. Petersen,et al.  Memory's echo: vivid remembering reactivates sensory-specific cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[23]  JaneR . Taylor,et al.  Bidirectional behavioral plasticity of memory reconsolidation depends on amygdalar protein kinase A , 2006, Nature Neuroscience.

[24]  E. Tulving,et al.  Toward a theory of episodic memory: the frontal lobes and autonoetic consciousness. , 1997, Psychological bulletin.

[25]  Joseph E LeDoux,et al.  Extinction Learning in Humans Role of the Amygdala and vmPFC , 2004, Neuron.

[26]  G. Quirk,et al.  Neurons in medial prefrontal cortex signal memory for fear extinction , 2002, Nature.

[27]  S. Hollon,et al.  6 – Cognitive Therapy of Depression1 , 1979 .

[28]  K. Scherer Psychological models of emotion. , 2000 .

[29]  B. Roozendaal,et al.  Stress doses of hydrocortisone, traumatic memories, and symptoms of posttraumatic stress disorder in patients after cardiac surgery: a randomized study , 2004, Biological Psychiatry.

[30]  A. Goldman In Defense of the Simulation Theory , 1992 .

[31]  Evelyne Balteau,et al.  The Locus Ceruleus Is Involved in the Successful Retrieval of Emotional Memories in Humans , 2006, The Journal of Neuroscience.

[32]  Gordon H. Bower,et al.  Cognition And Emotion , 1996 .

[33]  G. Winocur,et al.  The cognitive neuroscience of remote episodic, semantic and spatial memory , 2006, Current Opinion in Neurobiology.

[34]  A. Thiel,et al.  Right amygdalar and temporofrontal activation during autobiographic, but not during fictitious memory retrieval. , 2000, Behavioural neurology.

[35]  D. D. de Quervain,et al.  Glucocorticoids reduce phobic fear in humans. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[36]  R. Stickgold,et al.  Dissociable stages of human memory consolidation and reconsolidation , 2003, Nature.

[37]  R. Dolan,et al.  A subcortical pathway to the right amygdala mediating "unseen" fear. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[38]  Michael Davis,et al.  The amygdala: vigilance and emotion , 2001, Molecular Psychiatry.

[39]  S. Taylor,et al.  The Effect of Emotional Content on Visual Recognition Memory: A PET Activation Study , 1998, NeuroImage.

[40]  S. Guttenplan Mind and language , 1975 .

[41]  Elizabeth A. Kensinger,et al.  Memory enhancement for emotional words: Are emotional words more vividly remembered than neutral words? , 2003, Memory & cognition.

[42]  Yadin Dudai,et al.  Reconsolidation: the advantage of being refocused , 2006, Current Opinion in Neurobiology.

[43]  E. Eich Searching for Mood Dependent Memory , 1995 .

[44]  Michael D. Rugg,et al.  Recognition memory for emotionally negative and neutral words: an ERP study , 2000, Neuropsychologia.

[45]  Herbert F. Crovitz,et al.  Frequency of episodic memories as a function of their age , 1974 .

[46]  M L Russell,et al.  Differential effects of induced mood on the recall of positive, negative and neutral words. , 1983, The British journal of clinical psychology.

[47]  Stephen G. Gilligan,et al.  Emotional Mood as a Context for Learning and Recall. , 1978 .

[48]  Joseph E LeDoux,et al.  Differential contribution of dorsal and ventral medial prefrontal cortex to the acquisition and extinction of conditioned fear in rats. , 1995, Behavioral neuroscience.

[49]  J. D. McGaugh,et al.  Modulation of memory storage , 1996, Current Opinion in Neurobiology.

[50]  M. Packard,et al.  Affective modulation of multiple memory systems , 2001, Current Opinion in Neurobiology.

[51]  H. Lanfermann,et al.  Engagement of Lateral and Medial Prefrontal Areas in the Ecphory of Sad and Happy Autobiographical Memories , 2003, Cortex.

[52]  B. Knowlton,et al.  Remembering episodes: a selective role for the hippocampus during retrieval , 2000, Nature Neuroscience.

[53]  R. Dolan,et al.  Distant influences of amygdala lesion on visual cortical activation during emotional face processing , 2004, Nature Neuroscience.

[54]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[55]  Michael Davis,et al.  Behavioral and Neural Analysis of Extinction , 2002, Neuron.

[56]  S. Sara Retrieval and reconsolidation: toward a neurobiology of remembering. , 2000, Learning & memory.

[57]  Stephen Maren,et al.  Hippocampal Inactivation Disrupts Contextual Retrieval of Fear Memory after Extinction , 2001, The Journal of Neuroscience.

[58]  R. Adolphs,et al.  Memories for emotional autobiographical events following unilateral damage to medial temporal lobe. , 2006, Brain : a journal of neurology.

[59]  E. Phelps Human emotion and memory: interactions of the amygdala and hippocampal complex , 2004, Current Opinion in Neurobiology.

[60]  B. Underwood Attributes of Memory , 1983 .

[61]  R. Cabeza,et al.  Cognitive neuroscience of emotional memory , 2006, Nature Reviews Neuroscience.

[62]  Suparna Rajaram,et al.  Remembering and knowing: Two means of access to the personal past , 1993, Memory & cognition.

[63]  P. Hertel Memory for Emotional and Nonemotional Events in Depression: A Question of Habit? , 2004 .

[64]  D. Paré,et al.  Stimulation of Medial Prefrontal Cortex Decreases the Responsiveness of Central Amygdala Output Neurons , 2003, The Journal of Neuroscience.

[65]  Michael D Rugg,et al.  Remembrance of Odors Past Human Olfactory Cortex in Cross-Modal Recognition Memory , 2004, Neuron.

[66]  Richard N A Henson,et al.  Modulation of retrieval processing reflects accuracy of emotional source memory. , 2005, Learning & memory.

[67]  P. A. Lewis,et al.  Brain mechanisms for mood congruent memory facilitation , 2005, NeuroImage.

[68]  Jordan Grafman,et al.  Handbook of Neuropsychology , 1991 .

[69]  Karim Nader,et al.  Memory traces unbound , 2003, Trends in Neurosciences.

[70]  J. Forgas Mood and judgment: the affect infusion model (AIM). , 1995, Psychological bulletin.

[71]  D. J. Lewis,et al.  Retrograde Amnesia Produced by Electroconvulsive Shock after Reactivation of a Consolidated Memory Trace , 1968, Science.

[72]  D. Rubin,et al.  Distribution of important and word-cued autobiographical memories in 20-, 35-, and 70-year-old adults. , 1997, Psychology and aging.

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

[74]  S. Kosslyn,et al.  Neural foundations of imagery , 2001, Nature Reviews Neuroscience.

[75]  R. Dolan,et al.  Differential activation of the prefrontal cortex in successful and unsuccessful memory retrieval. , 1996, Brain : a journal of neurology.

[76]  Endel Tulving,et al.  Encoding specificity and retrieval processes in episodic memory. , 1973 .

[77]  D. Rubin,et al.  Emotionally charged autobiographical memories across the life span: the recall of happy, sad, traumatic, and involuntary memories. , 2002, Psychology and aging.

[78]  T. Seidenbecher,et al.  Amygdalar and Hippocampal Theta Rhythm Synchronization During Fear Memory Retrieval , 2003, Science.

[79]  The startled seahorse: Is the hippocampus necessary for contextual fear conditioning? , 1998 .

[80]  M. Bradley,et al.  Affective picture processing: the late positive potential is modulated by motivational relevance. , 2000, Psychophysiology.

[81]  Henry L. Roediger,et al.  Distortions of memory , 2000 .

[82]  R. Buckner,et al.  THE COGNITIVE NEUROSCIENCE OF REMEMBERING , 2001 .

[83]  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.

[84]  J. Mazziotta,et al.  Cortical mechanisms of human imitation. , 1999, Science.

[85]  H. Karnath,et al.  Using human brain lesions to infer function: a relic from a past era in the fMRI age? , 2004, Nature Reviews Neuroscience.

[86]  D. Rubin,et al.  Brain Activity during Episodic Retrieval of Autobiographical and Laboratory Events: An fMRI Study using a Novel Photo Paradigm , 2004, Journal of Cognitive Neuroscience.

[87]  Daniel L Schacter,et al.  Amygdala Activity Is Associated with the Successful Encoding of Item, But Not Source, Information for Positive and Negative Stimuli , 2006, The Journal of Neuroscience.

[88]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[89]  E. Tulving,et al.  Reactivation of encoding-related brain activity during memory retrieval. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[90]  R. Henson,et al.  Neural activity associated with episodic memory for emotional context , 2001, Neuropsychologia.

[91]  Endel Tulving,et al.  Encoding and retrieval of information , 2000 .

[92]  G. Bower,et al.  In search of mood-dependent retrieval. , 1989 .

[93]  L R Squire,et al.  Retrograde Amnesia for Facts and Events: Findings from Four New Cases , 1998, The Journal of Neuroscience.

[94]  Daniel Reisberg,et al.  Memory and emotion. , 2004 .

[95]  Michael D. Rugg,et al.  Event-Related Potential Correlates of the Retrieval of Emotional and Nonemotional Context , 2004, Journal of Cognitive Neuroscience.

[96]  G. Fink,et al.  Cerebral Representation of One’s Own Past: Neural Networks Involved in Autobiographical Memory , 1996, The Journal of Neuroscience.

[97]  L. Nadel,et al.  Memory consolidation, retrograde amnesia and the hippocampal complex , 1997, Current Opinion in Neurobiology.

[98]  R. Dolan,et al.  Task and Content Modulate Amygdala-Hippocampal Connectivity in Emotional Retrieval , 2006, Neuron.

[99]  Kevin S. LaBar,et al.  Co-activation of the amygdala, hippocampus and inferior frontal gyrus during autobiographical memory retrieval , 2005, Neuropsychologia.

[100]  J. Gore,et al.  Activation of the left amygdala to a cognitive representation of fear , 2001, Nature Neuroscience.

[101]  Erik W. Moody,et al.  Memory processes in classical conditioning , 2004, Neuroscience & Biobehavioral Reviews.

[102]  E. Tulving,et al.  Task-related and item-related brain processes of memory retrieval. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[103]  Tali Sharot,et al.  How emotion enhances the feeling of remembering , 2004, Nature Neuroscience.

[104]  Michael Davis,et al.  Blocking of acquisition but not expression of conditioned fear-potentiated startle by NMDA antagonists in the amygdala , 1990, Nature.

[105]  P. H. Blaney Affect and memory: a review. , 1986, Psychological bulletin.

[106]  K. Nader,et al.  Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval , 2000, Nature.

[107]  Ramona O Hopkins,et al.  Successful Recollection of Remote Autobiographical Memories by Amnesic Patients with Medial Temporal Lobe Lesions , 2003, Neuron.

[108]  John D. Bransford,et al.  Levels of processing versus transfer appropriate processing , 1977 .

[109]  Benjamin J. Shannon,et al.  Parietal lobe contributions to episodic memory retrieval , 2005, Trends in Cognitive Sciences.

[110]  E. Rolls,et al.  Abstract reward and punishment representations in the human orbitofrontal cortex , 2001, Nature Neuroscience.

[111]  J. Williams,et al.  Autobiographical memory in depression , 1988, Psychological Medicine.

[112]  R. Cabeza,et al.  Interaction between the Amygdala and the Medial Temporal Lobe Memory System Predicts Better Memory for Emotional Events , 2004, Neuron.

[113]  F. Craik,et al.  Hemispheric encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[114]  Gereon R Fink,et al.  Gender differences in the functional neuroanatomy of emotional episodic autobiographical memory , 2005, Human brain mapping.

[115]  Morris Moscovitch,et al.  Recollective qualities modulate hippocampal activation during autobiographical memory retrieval , 2004, Hippocampus.

[116]  L R Squire,et al.  Reactivation of recent or remote memory before electroconvulsive therapy does not produce retrograde amnesia. , 1976, Behavioral biology.

[117]  Martin Lepage,et al.  A Process-specific Functional Dissociation of the Amygdala in Emotional Memory , 2006, Journal of Cognitive Neuroscience.

[118]  A. Koriat,et al.  What do we know about what we cannot remember? Accessing the semantic attributes of words that cannot be recalled. , 2003, Journal of experimental psychology. Learning, memory, and cognition.

[119]  R. Dolan,et al.  Human orbitofrontal cortex mediates extinction learning while accessing conditioned representations of value , 2004, Nature Neuroscience.

[120]  E A Maguire,et al.  Neuroimaging studies of autobiographical event memory. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[121]  H. Heinze,et al.  Recapitulating emotional context: activity of amygdala, hippocampus and fusiform cortex during recollection and familiarity , 2005, The European journal of neuroscience.

[122]  R. Cabeza,et al.  Remembering one year later: role of the amygdala and the medial temporal lobe memory system in retrieving emotional memories. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[123]  M. Kozak,et al.  Emotional processing of fear: exposure to corrective information. , 1986, Psychological bulletin.

[124]  M. Bouton,et al.  Contextual and Temporal Modulation of Extinction: Behavioral and Biological Mechanisms , 2006, Biological Psychiatry.

[125]  R. Adolphs,et al.  Emotion recognition from faces and prosody following temporal lobectomy. , 2001, Neuropsychology.

[126]  Matthew L. Shapiro,et al.  Retrieving Memories via Internal Context Requires the Hippocampus , 2004, The Journal of Neuroscience.

[127]  Ming Ouyang,et al.  A requirement for memory retrieval during and after long-term extinction learning. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[128]  J. Borod The Neuropsychology of emotion , 2000 .

[129]  Michael D. Rugg,et al.  Event-related potential studies of memory , 2000 .

[130]  Michael D. Rugg,et al.  Neural correlates of differential retrieval orientation: Sustained and item-related components , 2006, Neuropsychologia.

[131]  Gordon H. Bower,et al.  Affect, memory, and social cognition. , 2000 .

[132]  Lesley K. Fellows,et al.  Method Matters: An Empirical Study of Impact in Cognitive Neuroscience , 2005, Journal of Cognitive Neuroscience.

[133]  P. Schyns,et al.  A mechanism for impaired fear recognition after amygdala damage , 2005, Nature.

[134]  J. Teasdale,et al.  Differential effects of induced mood on retrieval of pleasant and unpleasant events from episodic memory. , 1979, Journal of abnormal psychology.

[135]  S. Kosslyn,et al.  Topographical representations of mental images in primary visual cortex , 1995, Nature.

[136]  G. Bower Mood and memory. , 1981, The American psychologist.

[137]  Kjell Elenius,et al.  Emotion Recognition , 2009, Computers in the Human Interaction Loop.

[138]  R. Adolphs,et al.  Emotional Autobiographical Memories in Amnesic Patients with Medial Temporal Lobe Damage , 2005, The Journal of Neuroscience.

[139]  John Patrick Aggleton,et al.  The Amygdala : a functional analysis , 2000 .

[140]  J. Borod Emotion and the brain—anatomy and theory: An introduction to the Special Section. , 1993 .

[141]  Tony W. Buchanan,et al.  The Neuroanatomy of Emotional Memory in Humans. , 2004 .

[142]  D. Rubin,et al.  PSYCHOLOGICAL SCIENCE Research Article CONFIDENCE, NOT CONSISTENCY, CHARACTERIZES FLASHBULB MEMORIES , 2001 .

[143]  F. Craik,et al.  The Oxford handbook of memory , 2006 .

[144]  M. Rugg,et al.  Separating the Brain Regions Involved in Recollection and Familiarity in Recognition Memory , 2005, The Journal of Neuroscience.

[145]  D. Murphy,et al.  Mood-state-dependent retrieval of verbal associations. , 1977, Journal of abnormal psychology.

[146]  K. Luan Phan,et al.  Functional Neuroanatomy of Emotion: A Meta-Analysis of Emotion Activation Studies in PET and fMRI , 2002, NeuroImage.

[147]  R T Knight,et al.  Recollection and familiarity deficits in amnesia: convergence of remember-know, process dissociation, and receiver operating characteristic data. , 1998, Neuropsychology.

[148]  Y. Dudai The neurobiology of consolidations, or, how stable is the engram? , 2004, Annual review of psychology.

[149]  Rugg,et al.  Recollection and familiarity in recognition memory: an event-related fMRI study , 1999 .

[150]  Gereon R Fink,et al.  Differential remoteness and emotional tone modulate the neural correlates of autobiographical memory. , 2003, Brain : a journal of neurology.

[151]  G. Bower,et al.  Commentary on mood and memory. , 1987, Behaviour research and therapy.

[152]  J. D. McGaugh,et al.  The neurobiology of learning and memory: some reminders to remember , 2001, Trends in Neurosciences.

[153]  Jennifer M. Talarico,et al.  Emotional intensity predicts autobiographical memory experience , 2004, Memory & cognition.

[154]  H. Markowitsch Differential contribution of right and left amygdala to affective information processing. , 1998, Behavioural neurology.

[155]  P. Lang,et al.  A FEAR SURVEY SCHEDULE FOR USE IN BEHAVIOUR THERAPY. , 1964, Behaviour research and therapy.