Repeatedly reactivated memories become more resistant to hippocampal damage.

We examined whether repeated reactivations of a context memory would prevent the typical amnesic effects of post-training damage to the hippocampus (HPC). Rats were given a single contextual fear-conditioning session followed by 10 reactivations, involving a brief return to the conditioning context (no shock). Subsequently, the rats received sham or complete lesions of the HPC. When tested for retention, the HPC rats that experienced the reactivations froze significantly more than nonreactivation HPC rats and did not significantly differ from their respective control group. These findings suggest that memory reactivations contribute to long-term memories becoming independent of the HPC.

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

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

[3]  H. Eichenbaum,et al.  Dynamics of Hippocampal and Cortical Activation during Consolidation of a Nonspatial Memory , 2006, The Journal of Neuroscience.

[4]  R G Phillips,et al.  Contributions of postrhinal and perirhinal cortex to contextual information processing. , 2000, Behavioral neuroscience.

[5]  Jonathan L. C. Lee Reconsolidation: maintaining memory relevance , 2009, Trends in Neurosciences.

[6]  R. Sutherland,et al.  Hippocampus and retrograde amnesia in the rat model: A modest proposal for the situation of systems consolidation , 2010, Neuropsychologia.

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

[8]  G. Winocur,et al.  Memory formation and long-term retention in humans and animals: Convergence towards a transformation account of hippocampal–neocortical interactions , 2010, Neuropsychologia.

[9]  Joseph E LeDoux,et al.  De novo mRNA synthesis is required for both consolidation and reconsolidation of fear memories in the amygdala. , 2008, Learning & memory.

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

[11]  M. Fanselow,et al.  Temporally Graded Retrograde Amnesia of Contextual Fear after Hippocampal Damage in Rats: Within-Subjects Examination , 1999, The Journal of Neuroscience.

[12]  K. Franklin,et al.  Reconsolidation of a morphine place preference: Impact of the strength and age of memory on disruption by propranolol and midazolam , 2010, Behavioural Brain Research.

[13]  G. Winocur,et al.  Changes in context-specificity during memory reconsolidation: selective effects of hippocampal lesions. , 2009, Learning & memory.

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

[15]  L. Squire,et al.  The primate hippocampal formation: evidence for a time-limited role in memory storage. , 1990, Science.

[16]  L. Swanson The Rat Brain in Stereotaxic Coordinates, George Paxinos, Charles Watson (Eds.). Academic Press, San Diego, CA (1982), vii + 153, $35.00, ISBN: 0 125 47620 5 , 1984 .

[17]  B. Everitt,et al.  Reconsolidation of appetitive memories for both natural and drug reinforcement is dependent on {beta}-adrenergic receptors. , 2008, Learning & memory.

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

[19]  Jonathan L. C. Lee,et al.  Memory reconsolidation mediates the strengthening of memories by additional learning , 2008, Nature Neuroscience.

[20]  M. Fanselow,et al.  Modality-specific retrograde amnesia of fear. , 1992, Science.

[21]  P. Frankland,et al.  The organization of recent and remote memories , 2005, Nature Reviews Neuroscience.

[22]  R. Sutherland,et al.  Complete or partial hippocampal damage produces equivalent retrograde amnesia for remote contextual fear memories , 2007, The European journal of neuroscience.

[23]  R. O’Reilly,et al.  Conjunctive representations, the hippocampus, and contextual fear conditioning , 2001, Cognitive, affective & behavioral neuroscience.

[24]  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.

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

[26]  José María Delgado-García,et al.  From learning to forgetting: Behavioral, circuitry, and molecular properties define the different functional states of the recognition memory trace , 2010, Hippocampus.

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

[28]  Alcino J. Silva,et al.  The Involvement of the Anterior Cingulate Cortex in Remote Contextual Fear Memory , 2004, Science.

[29]  M. Fanselow,et al.  Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats , 1997, Behavioural Brain Research.

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

[31]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[32]  Dorothy Tse,et al.  References and Notes Supporting Online Material Materials and Methods Figs. S1 to S5 Tables S1 to S3 Electron Impact (ei) Mass Spectra Chemical Ionization (ci) Mass Spectra References Schemas and Memory Consolidation Research Articles Research Articles Research Articles Research Articles , 2022 .

[33]  I. Whishaw,et al.  Similar development of cued and learned home bases in control and hippocampal‐damaged rats in an open field exploratory task , 2007, Hippocampus.

[34]  Karim Nader,et al.  A bridge over troubled water: reconsolidation as a link between cognitive and neuroscientific memory research traditions. , 2010, Annual review of psychology.

[35]  M. Fanselow,et al.  Selective impairment of long-term but not short-term conditional fear by the N-methyl-D-aspartate antagonist APV. , 1992, Behavioral neuroscience.

[36]  R. Sutherland,et al.  Absence of systems consolidation of fear memories after dorsal, ventral, or complete hippocampal damage , 2008, Hippocampus.

[37]  Fraser T. Sparks,et al.  Making context memories independent of the hippocampus. , 2009, Learning & memory.

[38]  Fraser T. Sparks,et al.  Retrograde amnesia for fear-potentiated startle in rats after complete, but not partial, hippocampal damage , 2010, Neuroscience.

[39]  R. Clark,et al.  Object recognition memory and the rodent hippocampus. , 2010, Learning & memory.

[40]  Christof Koch,et al.  Inverse temporal contributions of the dorsal hippocampus and medial prefrontal cortex to the expression of long-term fear memories. , 2008, Learning & memory.

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

[42]  G. Winocur Anterograde and retrograde amnesia in rats with dorsal hippocampal or dorsomedial thalamic lesions , 1990, Behavioural Brain Research.

[43]  P. Frankland,et al.  The precision of remote context memories does not require the hippocampus , 2009, Nature Neuroscience.

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

[45]  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.