The spatiotemporal dynamics of autobiographical memory: neural correlates of recall, emotional intensity, and reliving.

We sought to map the time course of autobiographical memory retrieval, including brain regions that mediate phenomenological experiences of reliving and emotional intensity. Participants recalled personal memories to auditory word cues during event-related functional magnetic resonance imaging (fMRI). Participants pressed a button when a memory was accessed, maintained and elaborated the memory, and then gave subjective ratings of emotion and reliving. A novel fMRI approach based on timing differences capitalized on the protracted reconstructive process of autobiographical memory to segregate brain areas contributing to initial access and later elaboration and maintenance of episodic memories. The initial period engaged hippocampal, retrosplenial, and medial and right prefrontal activity, whereas the later period recruited visual, precuneus, and left prefrontal activity. Emotional intensity ratings were correlated with activity in several regions, including the amygdala and the hippocampus during the initial period. Reliving ratings were correlated with activity in visual cortex and ventromedial and inferior prefrontal regions during the later period. Frontopolar cortex was the only brain region sensitive to emotional intensity across both periods. Results were confirmed by time-locked averages of the fMRI signal. The findings indicate dynamic recruitment of emotion-, memory-, and sensory-related brain regions during remembering and their dissociable contributions to phenomenological features of the memories.

[1]  D. Amaral,et al.  Macaque monkey retrosplenial cortex: III. Cortical efferents , 2003, The Journal of comparative neurology.

[2]  B. Levine,et al.  The functional neuroanatomy of autobiographical memory: A meta-analysis , 2006, Neuropsychologia.

[3]  David C. Rubin,et al.  The Basic-Systems Model of Episodic Memory , 2006, Perspectives on psychological science : a journal of the Association for Psychological Science.

[4]  Rossana de Beni,et al.  Left mediotemporal structures mediate the retrieval of episodic autobiographical mental images , 2006, NeuroImage.

[5]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[6]  R. Cabeza,et al.  Cerebral Cortex doi:10.1093/cercor/bhj097 Role of Prefrontal and Anterior Cingulate Regions in Decision-Making Processes Shared by Memory and Nonmemory Tasks , 2005 .

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

[8]  A. Wagner,et al.  Domain-general and domain-sensitive prefrontal mechanisms for recollecting events and detecting novelty. , 2005, Cerebral cortex.

[9]  Mary L. Phillips,et al.  A Double Dissociation of Ventromedial Prefrontal Cortical Responses to Sad and Happy Stimuli in Depressed and Healthy Individuals , 2005, Biological Psychiatry.

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

[11]  Adrian M Owen,et al.  Distinct roles for lateral and medial anterior prefrontal cortex in contextual recollection. , 2005, Journal of neurophysiology.

[12]  G. Winocur,et al.  Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory , 2005, Journal of anatomy.

[13]  David C. Rubin,et al.  A Basic-Systems Approach to Autobiographical Memory , 2005 .

[14]  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.

[15]  Roberto Cabeza,et al.  Neural Correlates of Relational Memory: Successful Encoding and Retrieval of Semantic and Perceptual Associations , 2005, The Journal of Neuroscience.

[16]  Asaf Gilboa,et al.  Autobiographical and episodic memory—one and the same? Evidence from prefrontal activation in neuroimaging studies , 2004, Neuropsychologia.

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

[18]  K. Phan,et al.  Neural correlates of internally-generated disgust via autobiographical recall: a functional magnetic resonance imaging investigation , 2004, Neuroscience Letters.

[19]  Benjamin J. Shannon,et al.  Functional-Anatomic Correlates of Memory Retrieval That Suggest Nontraditional Processing Roles for Multiple Distinct Regions within Posterior Parietal Cortex , 2004, The Journal of Neuroscience.

[20]  G. Winocur,et al.  Remembering our past: functional neuroanatomy of recollection of recent and very remote personal events. , 2004, Cerebral cortex.

[21]  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.

[22]  D. Rubin,et al.  Facets of personality and the phenomenology of autobiographical memory , 2004 .

[23]  Kevin S LaBar,et al.  Emotional intensity predicts autobiographical memory experience , 2004, Memory & cognition.

[24]  H. Eichenbaum Hippocampus Cognitive Processes and Neural Representations that Underlie Declarative Memory , 2004, Neuron.

[25]  R. Clark,et al.  The medial temporal lobe. , 2004, Annual review of neuroscience.

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

[27]  L. Davachi,et al.  Behavioral/systems/cognitive Functional–neuroanatomic Correlates of Recollection: Implications for Models of Recognition Memory , 2022 .

[28]  Mark E Wheeler,et al.  Functional-anatomic correlates of remembering and knowing , 2004, NeuroImage.

[29]  S. Corkin,et al.  Two routes to emotional memory: distinct neural processes for valence and arousal. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

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

[31]  Dick J Veltman,et al.  Common pathway in the medial temporal lobe for storage and recovery of words as revealed by event‐related functional MRI , 2004, Hippocampus.

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

[33]  David C. Rubin,et al.  The Neuropsychology of Autobiographical Memory , 2003, Cortex.

[34]  Sharron E. Whitecross,et al.  Neurophysiological correlates of memory for experienced and imagined events , 2003, Neuropsychologia.

[35]  M. Witter,et al.  Contributions of Thalamic Nuclei to Declarative Memory Functioning , 2003, Cortex.

[36]  Jesper Andersson,et al.  Isolating the retrieval of imagined pictures during episodic memory: activation of the left precuneus and left prefrontal cortex , 2003, NeuroImage.

[37]  Randy L. Buckner,et al.  Functional–Anatomic Correlates of Sustained and Transient Processing Components Engaged during Controlled Retrieval , 2003, The Journal of Neuroscience.

[38]  Masao Yukie,et al.  Differential thalamic connections of the posteroventral and dorsal posterior cingulate gyrus in the monkey , 2003, The European journal of neuroscience.

[39]  David C. Rubin,et al.  Belief and recollection of autobiographical memories , 2003, Memory & cognition.

[40]  Eleanor A Maguire,et al.  Lateral Asymmetry in the Hippocampal Response to the Remoteness of Autobiographical Memories , 2003, The Journal of Neuroscience.

[41]  Randy L Buckner,et al.  Functional–Anatomic Correlates of Control Processes in Memory , 2003, The Journal of Neuroscience.

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

[43]  D. Amaral,et al.  Macaque monkey retrosplenial cortex: II. Cortical afferents , 2003, The Journal of comparative neurology.

[44]  J. Raaijmakers,et al.  Neuroanatomical correlates of episodic encoding and retrieval in young and elderly subjects. , 2003, Brain : a journal of neurology.

[45]  E. Tulving Episodic memory: from mind to brain. , 2002, Annual review of psychology.

[46]  B L McNaughton,et al.  Coordinated Reactivation of Distributed Memory Traces in Primate Neocortex , 2002, Science.

[47]  Andrew P Yonelinas,et al.  Dissociating familiarity from recollection in human recognition memory: Different rates of forgetting over short retention intervals , 2002, Psychonomic bulletin & review.

[48]  Anthony D Wagner,et al.  Executive Control during Episodic Retrieval Multiple Prefrontal Processes Subserve Source Memory , 2002, Neuron.

[49]  C. N. Macrae,et al.  Finding the Self? An Event-Related fMRI Study , 2002, Journal of Cognitive Neuroscience.

[50]  D. Stuss,et al.  Adult clinical neuropsychology: lessons from studies of the frontal lobes. , 2002, Annual review of psychology.

[51]  D. Schacter,et al.  Prefrontal Contributions to Executive Control: fMRI Evidence for Functional Distinctions within Lateral Prefrontal Cortex , 2001, NeuroImage.

[52]  C W Pleydell-Pearce,et al.  The Neuroanatomy of Autobiographical Memory: A Slow Cortical Potential Study of Autobiographical Memory Retrieval ☆ , 2001 .

[53]  M Petrides,et al.  Selective activation of the ventrolateral prefrontal cortex in the human brain during active retrieval processing , 2001, The European journal of neuroscience.

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

[55]  N. Kapur,et al.  The loss of episodic memories in retrograde amnesia: single-case and group studies. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[56]  A. Yonelinas Components of episodic memory: the contribution of recollection and familiarity. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[58]  Dick J. Veltman,et al.  Parahippocampal Activation during Successful Recognition of Words: A Self-Paced Event-Related fMRI Study , 2001, NeuroImage.

[59]  G. Shulman,et al.  Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function , 2001, Proceedings of the National Academy of Sciences of the United States of America.

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

[61]  Marcia K. Johnson,et al.  Left Anterior Prefrontal Activation Increases with Demands to Recall Specific Perceptual Information , 2000, The Journal of Neuroscience.

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

[63]  S. Petersen,et al.  Retrieval Success is Accompanied by Enhanced Activation in Anterior Prefrontal Cortex During Recognition Memory: An Event-Related fMRI Study , 2000, Journal of Cognitive Neuroscience.

[64]  T. Shallice,et al.  Confidence in Recognition Memory for Words: Dissociating Right Prefrontal Roles in Episodic Retrieval , 2000, Journal of Cognitive Neuroscience.

[65]  J. Gabrieli,et al.  Event-Related Activation in the Human Amygdala Associates with Later Memory for Individual Emotional Experience , 2000, The Journal of Neuroscience.

[66]  A. Damasio,et al.  Subcortical and cortical brain activity during the feeling of self-generated emotions , 2000, Nature Neuroscience.

[67]  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.

[68]  R. Buckner,et al.  Neural Correlates of Episodic Retrieval Success , 2000, NeuroImage.

[69]  R. Cabeza,et al.  Neural bases of learning and memory: functional neuroimaging evidence , 2000, Current opinion in neurology.

[70]  Marcia K. Johnson,et al.  fMRI investigations of left and right PFC contributions to episodic remembering , 2000, Psychobiology.

[71]  M. Conway,et al.  The construction of autobiographical memories in the self-memory system. , 2000, Psychological review.

[72]  G. Mangun,et al.  The neural mechanisms of top-down attentional control , 2000, Nature Neuroscience.

[73]  M. Rugg,et al.  Retrieval processing and episodic memory , 2000, Trends in Cognitive Sciences.

[74]  O. Andreassen,et al.  Mice Deficient in Cellular Glutathione Peroxidase Show Increased Vulnerability to Malonate, 3-Nitropropionic Acid, and 1-Methyl-4-Phenyl-1,2,5,6-Tetrahydropyridine , 2000, The Journal of Neuroscience.

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

[76]  R. Cabeza,et al.  Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies , 2000, Journal of Cognitive Neuroscience.

[77]  David J. Turk,et al.  A positron emission tomography (PET) study of autobiographical memory retrieval. , 1999, Memory.

[78]  T. Shallice,et al.  Recollection and Familiarity in Recognition Memory: An Event-Related Functional Magnetic Resonance Imaging Study , 1999, The Journal of Neuroscience.

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

[80]  A. Wagner,et al.  Working Memory Contributions to Human Learning and Remembering , 1999, Neuron.

[81]  R. Davidson,et al.  The functional neuroanatomy of emotion and affective style , 1999, Trends in Cognitive Sciences.

[82]  G. Winocur,et al.  In Search of the Self: A Positron Emission Tomography Study , 1999 .

[83]  Stephan Arndt,et al.  The cerebellum plays a role in conscious episodic memory retrieval , 1999, Human brain mapping.

[84]  M. Bradley,et al.  Affective Norms for English Words (ANEW): Instruction Manual and Affective Ratings , 1999 .

[85]  E. Tulving,et al.  Episodic memory and the self in a case of isolated retrograde amnesia. , 1998, Brain : a journal of neurology.

[86]  J. Desmond,et al.  Material‐specific lateralization of prefrontal activation during episodic encoding and retrieval , 1998, Neuroreport.

[87]  Marcia K. Johnson,et al.  Left prefrontal activation during episodic remembering: an event‐related fMRI study , 1998, Neuroreport.

[88]  J. Desmond,et al.  Prefrontal cortex and recognition memory. Functional-MRI evidence for context-dependent retrieval processes. , 1998, Brain : a journal of neurology.

[89]  D C Rubin,et al.  Visual memory-deficit amnesia: a distinct amnesic presentation and etiology. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[90]  D. Schacter,et al.  Functional–Anatomic Study of Episodic Retrieval Using fMRI I. Retrieval Effort versus Retrieval Success , 1998, NeuroImage.

[91]  G. Fink,et al.  Neural activation during selective attention to subjective emotional responses , 1997, Neuroreport.

[92]  D C Rubin,et al.  The distribution of autobiographical memories across the lifespan , 1997, Memory & cognition.

[93]  Morris Moscovitch,et al.  Strategic retrieval and the frontal lobes: Evidence from confabulation and amnesia , 1997, Neuropsychologia.

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

[95]  H. Markowitsch,et al.  Right temporofrontal cortex as critical locus for the ecphory of old episodic memories. , 1996, Journal of neurology, neurosurgery, and psychiatry.

[96]  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.

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

[98]  N. Alpert,et al.  Conscious recollection and the human hippocampal formation: evidence from positron emission tomography. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[99]  Joseph E LeDoux Emotional networks and motor control: a fearful view. , 1996, Progress in brain research.

[100]  A R McIntosh,et al.  Functional brain maps of retrieval mode and recovery of episodic information , 1995, Neuroreport.

[101]  E Tulving,et al.  Functional role of the prefrontal cortex in retrieval of memories: a PET study , 1995, Neuroreport.

[102]  Richard S. J. Frackowiak,et al.  The Mind's Eye—Precuneus Activation in Memory-Related Imagery , 1995, NeuroImage.

[103]  Hans J. Markowitsch,et al.  Which brain regions are critically involved in the retrieval of old episodic memory? , 1995, Brain Research Reviews.

[104]  M Moscovitch,et al.  Recovered consciousness: a hypothesis concerning modularity and episodic memory. , 1995, Journal of clinical and experimental neuropsychology.

[105]  P Alvarez,et al.  Memory consolidation and the medial temporal lobe: a simple network model. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[106]  D. Cicchetti Emotion and Adaptation , 1993 .

[107]  R. Lazarus Emotion and Adaptation , 1991 .

[108]  A. Damasio Time-locked multiregional retroactivation: A systems-level proposal for the neural substrates of recall and recognition , 1989, Cognition.

[109]  Marcia K. Johnson,et al.  Phenomenal characteristics of memories for perceived and imagined autobiographical events. , 1988, Journal of experimental psychology. General.

[110]  D. Reisberg,et al.  The quantity, not the quality, of affect predicts memory vividness , 1988 .

[111]  K. Scherer,et al.  The Relationship of Emotion to Cognition: A Functional Approach to a Semantic Controversy , 1987 .

[112]  E Valenstein,et al.  Retrosplenial amnesia. , 1987, Brain : a journal of neurology.

[113]  David C. Rubin,et al.  On the retention function for autobiographical memory , 1982 .

[114]  David C. Rubin,et al.  51 properties of 125 words: A unit analysis of verbal behavior , 1980 .

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

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

[117]  D. Spalding The Principles of Psychology , 1873, Nature.