Intrahippocampal anisomycin infusions disrupt previously consolidated spatial memory only when memory is updated

Reconsolidation has proven to be a common phenomenon relevant to memory processing. However, the functional significance of this process is still a matter of debate. Previous work has shown that reconsolidation is indeed a process by which updated information is integrated, through the synthesis of proteins, to a memory trace. To further analyze the role that updated information plays in retrieved spatial memory susceptibility to disruption, we injected anisomycin bilaterally in the dorsal hippocampus of Wistar rats. Implanted animals were trained for 5 days on the Morris water maze (MWM) task and injected with anisomycin before the third or fifth training session. When memory was assessed a week later, only animals injected on the third training session showed disruption of long-term memory. Furthermore, when animals were trained for either 3 (middle-trained) or 5 (well-trained) days and a week later anisomycin was infused before a reminder session, only middle-trained rats infused with anisomycin showed reduced performance when tested for long-term memory. Finally, animals trained for 5 days and injected with anisomycin 7 days later on an extinction session showed impaired long-term extinction when tested. These results suggest that for spatial memory tasks acquisition of updated information is a necessary feature to undergo this process. We propose that reconsolidation is not an accurate term because it implies that consolidation happens again. This conception does not fit with the evidence; hence, we suggest that updating consolidation is a more descriptive term to refer to this process.

[1]  J. Born,et al.  Elevated Sleep Spindle Density after Learning or after Retrieval in Rats , 2006, The Journal of Neuroscience.

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

[3]  R. Morris,et al.  Place navigation impaired in rats with hippocampal lesions , 1982, Nature.

[4]  K. Rosenblum,et al.  Lateral ventricle injection of the protein synthesis inhibitor anisomycin impairs long-term memory in a spatial memory task , 1998, Brain Research.

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

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

[7]  E. Kandel The Molecular Biology of Memory Storage: A Dialogue Between Genes and Synapses , 2001, Science.

[8]  H. Eichenbaum A cortical–hippocampal system for declarative memory , 2000, Nature Reviews Neuroscience.

[9]  A. Hupbach,et al.  Reconsolidation of episodic memories: a subtle reminder triggers integration of new information. , 2007, Learning & memory.

[10]  L. Mahadevan,et al.  Anisomycin Selectively Desensitizes Signalling Components Involved in Stress Kinase Activation and fos andjun Induction , 1998, Molecular and Cellular Biology.

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

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

[13]  B. Everitt,et al.  Cellular Imaging of zif268 Expression in the Hippocampus and Amygdala during Contextual and Cued Fear Memory Retrieval: Selective Activation of Hippocampal CA1 Neurons during the Recall of Contextual Memories , 2001, The Journal of Neuroscience.

[14]  F. Bermúdez-Rattoni,et al.  Protein synthesis underlies post-retrieval memory consolidation to a restricted degree only when updated information is obtained. , 2005, Learning & memory.

[15]  T. Bozorgmehr,et al.  The effects of anisomycin (a protein synthesis inhibitor) on spatial learning and memory in CA1 region of rats hippocampus , 2003, Behavioural Brain Research.

[16]  J L McGaugh,et al.  Antisense oligodeoxynucleotide-mediated disruption of hippocampal cAMP response element binding protein levels impairs consolidation of memory for water maze training. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[19]  J. D. McGaugh,et al.  Retrieval of memory for fear-motivated training initiates extinction requiring protein synthesis in the rat hippocampus , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[20]  S. Rose,et al.  Two time windows of anisomycin-induced amnesia for inhibitory avoidance training in rats: protection from amnesia by pretraining but not pre-exposure to the task apparatus. , 1999, Learning & memory.

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

[22]  K. Lukowiak,et al.  Reconsolidation and memory infidelity in Lymnaea , 2007, Neurobiology of Learning and Memory.

[23]  C. Alberini,et al.  Linking New Information to a Reactivated Memory Requires Consolidation and Not Reconsolidation Mechanisms , 2005, PLoS biology.

[24]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[25]  P. E. Gold,et al.  The many faces of amnesia. , 2006, Learning & memory.

[26]  Martín Cammarota,et al.  Retrieval induces hippocampal-dependent reconsolidation of spatial memory. , 2006, Learning & memory.

[27]  D. Lewis Psychobiology of active and inactive memory. , 1979 .

[28]  F. Bermúdez-Rattoni,et al.  Memory Reconsolidation or Updating Consolidation , 2007 .

[29]  R. Morris,et al.  Memory Reconsolidation: Sensitivity of Spatial Memory to Inhibition of Protein Synthesis in Dorsal Hippocampus during Encoding and Retrieval , 2006, Neuron.

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

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

[32]  Federico Bermúdez-Rattoni,et al.  Neural Plasticity and Memory , 2007 .

[33]  L. Squire,et al.  Protein synthesis and memory: a review. , 1984, Psychological bulletin.

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

[35]  Martín Cammarota,et al.  On the role of hippocampal protein synthesis in the consolidation and reconsolidation of object recognition memory. , 2007, Learning & memory.

[36]  S. Davis,et al.  Activation of Mitogen-Activated Protein Kinase/Extracellular Signal-Regulated Kinase in Hippocampal Circuitry Is Required for Consolidation and Reconsolidation of Recognition Memory , 2003, The Journal of Neuroscience.

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

[38]  S. Tronel,et al.  Mapping of olfactory memory circuits: region-specific c-fos activation after odor-reward associative learning or after its retrieval. , 2002, Learning & memory.

[39]  J L McGaugh,et al.  Time-Dependent Processes in Memory Storage , 1966, Science.