Reactivation, Retrieval, Replay and Reconsolidation in and Out of Sleep: Connecting the Dots

The neurobiology of memory has taken on a new look over the past decade. Re-discovery of cue-dependent amnesia, wide availability of functional imaging tools and increased dialog among clinicians, cognitive psychologists, behavioral neuroscientists, and neurobiologists have provided impetus for the search for new paradigms for the study of memory. Memory is increasingly viewed as an open-ended process, with retrieval being recognized as an intricate part of the encoding process. New memories are always made on the background of past experience, so that every consolidation is, in fact reconsolidation, serving to update and strengthen memories after retrieval. Spontaneous reactivation of memory circuits occurs during sleep and there is converging evidence from rodent and human studies that this is an important part of the extended off-line memory processing. The noradrenergic neuromodulatory system is engaged at retrieval, facilitating recall. The noradrenergic system is also activated during sleep after learning and noradrenergic neurons fire in concert with cortical oscillations that are associated with reactivation of memory circuits. We suggest that the noradrenergic system and perhaps other neuromodulatory systems, may be a key to linking off-line memory reactivation, retrieval, and memory reconsolidation processes at both synaptic and systems levels, in and out of sleep.

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

[2]  Joseph E LeDoux,et al.  Noradrenergic Signaling in the Amygdala Contributes to the Reconsolidation of Fear Memory , 2006, Annals of the New York Academy of Sciences.

[3]  K. Nader,et al.  Memory reconsolidation: an update , 2010, Annals of the New York Academy of Sciences.

[4]  S. Sara,et al.  Idazoxan, an alpha-2 antagonist, facilitates memory retrieval in the rat. , 1989, Behavioral and neural biology.

[5]  W. Fishbein,et al.  Disruptive effects of rapid eye movement sleep deprivation on long-term memory. , 1971, Physiology & behavior.

[6]  M. Steriade,et al.  Neuronal Plasticity in Thalamocortical Networks during Sleep and Waking Oscillations , 2003, Neuron.

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

[8]  J. D. McGaugh,et al.  Drug enhancement of memory consolidation: historical perspective and neurobiological implications , 2008, Psychopharmacology.

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

[10]  S. Sara,et al.  Commentary — reconsolidation: Strengthening the shaky trace through retrieval , 2000, Nature Reviews Neuroscience.

[11]  N. Spear.  Retrieval of memory in animals. , 1973 .

[12]  C. Pavlides,et al.  Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  Y. Dudai,et al.  Rites of Passage of the Engram Reconsolidation and the Lingering Consolidation Hypothesis , 2004, Neuron.

[14]  S. Tronel,et al.  Noradrenergic action in prefrontal cortex in the late stage of memory consolidation. , 2004, Learning & memory.

[15]  J. O’Neill,et al.  Play it again: reactivation of waking experience and memory , 2010, Trends in Neurosciences.

[16]  S. Sara,et al.  Priming stimulation of locus coeruleus facilitates memory retrieval in the rat , 1988, Brain Research.

[17]  H. J. Spiers,et al.  The neuroscience of remote spatial memory: A tale of two cities , 2007, Neuroscience.

[18]  E. Hennevin,et al.  Augmentation du sommeil paradoxal provoquée par l'acquisition, l'extinction et la réacquisition d'un apprentisageàrenforcement positif , 1974 .

[19]  S. Sara,et al.  Idazoxan, an α-2 antagonist, facilitates memory retrieval in the rat , 1989 .

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

[21]  B. McNaughton,et al.  Reactivation of Hippocampal Cell Assemblies: Effects of Behavioral State, Experience, and EEG Dynamics , 1999, The Journal of Neuroscience.

[22]  T. Robbins,et al.  The neuropsychopharmacology of fronto-executive function: monoaminergic modulation. , 2009, Annual review of neuroscience.

[23]  Oxana Eschenko,et al.  Learning-dependent, transient increase of activity in noradrenergic neurons of locus coeruleus during slow wave sleep in the rat: brain stem-cortex interplay for memory consolidation? , 2008, Cerebral cortex.

[24]  B. Hars,et al.  In memory of consolidation. , 2006, Learning & memory.

[25]  J. Born,et al.  Sustained increase in hippocampal sharp-wave ripple activity during slow-wave sleep after learning. , 2008, Learning & memory.

[26]  J. O’Neill,et al.  The reorganization and reactivation of hippocampal maps predict spatial memory performance , 2010, Nature Neuroscience.

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

[28]  JaneR . Taylor,et al.  Molecular mechanisms of memory reconsolidation , 2007, Nature Reviews Neuroscience.

[29]  P Roullet,et al.  Attenuation of Emotional and Nonemotional Memories after Their Reactivation: Role of ␤ Adrenergic Receptors , 1999 .

[30]  Yasushi Miyashita,et al.  Towards understanding of the cortical network underlying associative memory , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[31]  B. Hars,et al.  Improvement of learning by cueing during postlearning paradoxical sleep , 1985, Behavioural Brain Research.

[32]  S. Sara,et al.  Consolidation of Memory After its Reactivation: Involvement of β Noradrenergic Receptors in the Late Phase , 1998, Neural plasticity.

[33]  R. Stickgold,et al.  Cognitive replay of visuomotor learning at sleep onset: temporal dynamics and relationship to task performance. , 2010, Sleep.

[34]  C. Alberini.  The role of protein synthesis during the labile phases of memory: Revisiting the skepticism , 2008, Neurobiology of Learning and Memory.

[35]  Y. Miyashita.  Inferior temporal cortex: where visual perception meets memory. , 1993, Annual review of neuroscience.

[36]  E. Hennevin,et al.  [The function of paradoxical sleep: facts and theories]. , 1971, L'annee psychologique.

[37]  D. J. Lewis,et al.  Psychobiology of active and inactive memory. , 1979, Psychological bulletin.

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

[39]  S. Sara.  Reconsolidation: Historical Perspective and Theoretical Aspects , 2008 .

[40]  B. Hars,et al.  Contextual cues and memory retrieval in rats: Alleviation of forgetting by a pretest exposure to background stimuli , 1980 .

[41]  B. Hars,et al.  Reticular stimulation facilitates retrieval of a ‘forgotten’ maze habit , 1980, Neuroscience Letters.

[42]  S. Sara,et al.  Memory retrieval enhanced by amphetamine after a long retention interval. , 1982, Behavioral and neural biology.

[43]  D J Lewis,et al.  Cue-dependent amnesia in rats. , 1972, Journal of comparative and physiological psychology.

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

[45]  G. Buzsáki.  Two-stage model of memory trace formation: A role for “noisy” brain states , 1989, Neuroscience.

[46]  O. Hardt,et al.  A single standard for memory: the case for reconsolidation , 2009, Nature Reviews Neuroscience.

[47]  M. Wilson,et al.  Coordinated Interactions between Hippocampal Ripples and Cortical Spindles during Slow-Wave Sleep , 1998, Neuron.

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

[49]  D. Quartermain,et al.  Characteristics of retrograde amnesia following reactivation of memory in mice , 1982, Physiology & Behavior.

[50]  J. Born,et al.  Hippocampal sharp wave-ripples linked to slow oscillations in rat slow-wave sleep. , 2006, Journal of neurophysiology.

[51]  J. Born,et al.  Odor Cues During Slow-Wave Sleep Prompt Declarative Memory Consolidation , 2007, Science.

[52]  S. Sara,et al.  Hippocampal Sharp Wave/Ripples during Sleep for Consolidation of Associative Memory , 2009, PLoS ONE.

[53]  [Paradoxical sleep increase triggered by learning, extinction and relearning of a response based on a positive reinforcement]. , 1974, Brain research.

[54]  S. Sara,et al.  Memory retrieval enhancement by locus coeruleus stimulation: evidence for mediation by β-receptors , 1991, Behavioural Brain Research.

[55]  C. Harley.  Norepinephrine and the dentate gyrus. , 2007, Progress in brain research.

[56]  Marcia K. Johnson,et al.  Source monitoring 15 years later: what have we learned from fMRI about the neural mechanisms of source memory? , 2009, Psychological bulletin.

[57]  R. Stickgold,et al.  Sleep-dependent memory consolidation and reconsolidation. , 2007, Sleep medicine.

[58]  M. Wilson,et al.  Temporally Structured Replay of Awake Hippocampal Ensemble Activity during Rapid Eye Movement Sleep , 2001, Neuron.

[59]  J. Przybysławski,et al.  Reconsolidation of memory after its reactivation , 1997, Behavioural Brain Research.

[60]  Y. Miyashita,et al.  Neural representation of visual objects: encoding and top-down activation , 2000, Current Opinion in Neurobiology.

[61]  J. Csicsvari,et al.  Ensemble Patterns of Hippocampal CA3-CA1 Neurons during Sharp Wave–Associated Population Events , 2000, Neuron.

[62]  D J Lewis,et al.  Source of cues for cue-dependent amnesia in rats. , 1973, Journal of comparative and physiological psychology.