Reconsolidation of fresh, remote, and extinguished fear memory in medaka: old fears don't die

Long‐term fear memory in the medaka fish (Oryzias latipes) regains transient sensitivity to a consolidation blocker immediately after memory reactivation in retrieval (‘reconsolidation’). Here we show that reconsolidation occurs in fresh long‐term memories but not in remote memories, and that the apparent amnesia induced by blockade of reconsolidation can be reinstated by an unpaired reinforcer, a procedure that has no effect on amnesia induced by blockade of consolidation. Extinction memory also undergoes post‐reactivation reconsolidation, the blockade of which exposes the previously acquired fear. Hence in medaka, the process manifested in reconsolidation seems itself to consolidate; moreover, even when the post‐reactivation application of the consolidation blocker is still able to disrupt the memory, the conditioned fear does not seem to go away permanently.

[1]  C. Alberini,et al.  Temporally Graded Requirement for Protein Synthesis following Memory Reactivation , 2002, Neuron.

[2]  Yadin Dudai,et al.  Amygdalar circuits required for either consolidation or extinction of taste aversion memory are not required for reconsolidation , 2004, The European journal of neuroscience.

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

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

[5]  B. Everitt,et al.  Independent Cellular Processes for Hippocampal Memory Consolidation and Reconsolidation , 2004, Science.

[6]  M. Schartl,et al.  Medaka — a model organism from the far east , 2002, Nature Reviews Genetics.

[7]  G. Quirk,et al.  The Role of Ventromedial Prefrontal Cortex in the Recovery of Extinguished Fear , 2000, The Journal of Neuroscience.

[8]  Y. Ishikawa,et al.  Medakafish as a model system for vertebrate developmental genetics. , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[9]  B. Torres,et al.  Avoidance Response in Goldfish: Emotional and Temporal Involvement of Medial and Lateral Telencephalic Pallium , 2004, The Journal of Neuroscience.

[10]  M. Bouton Context, ambiguity, and unlearning: sources of relapse after behavioral extinction , 2002, Biological Psychiatry.

[11]  Cristina M. Alberini,et al.  The consolidation of new but not reactivated memory requires hippocampal C/EBPβ , 2001, Nature Neuroscience.

[12]  Erik W. Moody,et al.  Learning and memory: Interpretations of retrograde amnesia: old problems redux , 2001, Nature Reviews Neuroscience.

[13]  B. O'Shea Post-traumatic stress disorder: A review for the general psychiatrist , 2001, International journal of psychiatry in clinical practice.

[14]  S. J. Martin,et al.  Forgetting, Reminding, and Remembering: The Retrieval of Lost Spatial Memory , 2004, PLoS biology.

[15]  J. Radulovic,et al.  Distinct Roles of Hippocampal De Novo Protein Synthesis and Actin Rearrangement in Extinction of Contextual Fear , 2004, The Journal of Neuroscience.

[16]  Y. Dudai,et al.  Stability of Retrieved Memory: Inverse Correlation with Trace Dominance , 2003, Science.

[17]  R. Rescorla Preservation of Pavlovian Associations through Extinction , 1996 .

[18]  D. Riccio,et al.  Retrograde amnesia for old (reactivated) memory: some anomalous characteristics. , 1979, Science.

[19]  Y. Dudai,et al.  Conflicting processes in the extinction of conditioned taste aversion: behavioral and molecular aspects of latency, apparent stagnation, and spontaneous recovery. , 2003, Learning & memory.

[20]  James L. McClelland,et al.  Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. , 1995, Psychological review.

[21]  Alcino J. Silva,et al.  Memory Reconsolidation and Extinction Have Distinct Temporal and Biochemical Signatures , 2004, The Journal of Neuroscience.

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

[23]  Joseph E LeDoux,et al.  Cellular and Systems Reconsolidation in the Hippocampus , 2002, Neuron.

[24]  K. V. Anokhin,et al.  Mechanisms of Memory Reorganization during Retrieval of Acquired Behavioral Experience in Chicks: the Effects of Protein Synthesis Inhibition in the Brain , 2000, Neuroscience and Behavioral Physiology.

[25]  P. E. Gold,et al.  Retrograde Amnesia and the "Reminder Effect": An Alternative Interpretation , 1973, Science.

[26]  Michael E. Hasselmo,et al.  A Proposed Function for Hippocampal Theta Rhythm: Separate Phases of Encoding and Retrieval Enhance Reversal of Prior Learning , 2002, Neural Computation.

[27]  Mark E. Bouton,et al.  Sources of relapse after extinction in Pavlovian and instrumental learning , 1991 .

[28]  M. E. Pedreira,et al.  Protein Synthesis Subserves Reconsolidation or Extinction Depending on Reminder Duration , 2003, Neuron.

[29]  S. Rose,et al.  Reminder effects: the molecular cascade following a reminder in young chicks does not recapitulate that following training on a passive avoidance task , 2004, The European journal of neuroscience.

[30]  F. Rodríguez,et al.  Spatial memory and hippocampal pallium through vertebrate evolution: insights from reptiles and teleost fish , 2002, Brain Research Bulletin.

[31]  D. Caine Memory from A to Z: Keywords, Concepts and Beyond Yadin Dudai Memory from A to Z: Keywords, Concepts and Beyond , 2005, Journal of Clinical Neuroscience.

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

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

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

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

[36]  Isaac Marks Fears, phobias, and rituals , 1987 .

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

[38]  Satoshi Kida,et al.  CREB required for the stability of new and reactivated fear memories , 2002, Nature Neuroscience.

[39]  S. Rose,et al.  Reminder effects – reconsolidation or retrieval deficit? Pharmacological dissection with protein synthesis inhibitors following reminder for a passive‐avoidance task in young chicks , 2002, The European journal of neuroscience.

[40]  S. Y. Wang,et al.  Charged tetracaine as an inactivation enhancer in batrachotoxin-modified Na+ channels. , 1994, Biophysical journal.