Erratum to: Comparative dynamics of MAPK/ERK signalling components and immediate early genes in the hippocampus and amygdala following contextual fear conditioning and retrieval

Over the past few years multiple studies have attempted to uncover molecular signatures of memory reconsolidation when compared to consolidation. In the present study we used immunocytochemical detection of the MAPK/ERK1/2 pathway, to track activated neuronal circuits in the hippocampus and amygdala recruited during the consolidation and reconsolidation of a contextual fear conditioning (CFC) memory. We report selective differences in magnitude and temporal dynamics of activated ERK1/2 signalling in different subregions of these two structures between the post-training and post-retrieval periods, except in the dentate gyrus, where the patterns of activation were similar. We then focused on this brain area to dissect out the patterns of downstream ERK1/2 signalling components, including the phosphorylation of MSK-1 and histone H3 on ser10, along with the induction of the Immediate Early Genes (IEGs) Arc/Arg3.1, c-Fos and Zif268/Egr1 following CFC training and retrieval. We found that the completion of the nucleosomal response as well as the induction of IEGs shorter during the reconsolidation period as compared to consolidation. Our results shed new light on the cellular mechanisms underlying the consolidation and reconsolidation processes engaged following CFC training and retrieval and further extend the notion that memory reconsolidation is not mechanistically a repetition of consolidation. In addition, we provide evidence that the strength of a previously established CFC memory is characterized by distinct patterns of ERK1/2 activation in different hippocampal and amygdalar subfields upon CFC memory recall. Our results emphasize the differences between consolidation and reconsolidation processes in relation to contextual fear memories.

[1]  P. Strata,et al.  Learning-related feedforward inhibitory connectivity growth required for memory precision , 2011, Nature.

[2]  Armin Schumacher,et al.  The Nuclear Kinase Mitogen- and Stress-Activated Protein Kinase 1 Regulates Hippocampal Chromatin Remodeling in Memory Formation , 2007, The Journal of Neuroscience.

[3]  Joseph E LeDoux,et al.  Why We Think Plasticity Underlying Pavlovian Fear Conditioning Occurs in the Basolateral Amygdala , 1999, Neuron.

[4]  J. Sweatt,et al.  ERK/MAPK regulates hippocampal histone phosphorylation following contextual fear conditioning. , 2006, Learning & memory.

[5]  B. McNaughton,et al.  Mapping behaviorally relevant neural circuits with immediate-early gene expression , 2005, Current Opinion in Neurobiology.

[6]  O. Amaral,et al.  A Mismatch-Based Model for Memory Reconsolidation and Extinction in Attractor Networks , 2011, PloS one.

[7]  H. Okuno,et al.  Synaptic activity-responsive element in the Arc/Arg3.1 promoter essential for synapse-to-nucleus signaling in activated neurons , 2009, Proceedings of the National Academy of Sciences.

[8]  K L Thomas,et al.  Fear memory retrieval induces CREB phosphorylation and Fos expression within the amygdala , 2001, The European journal of neuroscience.

[9]  J. David Sweatt,et al.  The MAPK cascade is required for mammalian associative learning , 1998, Nature Neuroscience.

[10]  Joseph E LeDoux,et al.  Synapse-specific reconsolidation of distinct fear memories in the lateral amygdala , 2007, Nature Neuroscience.

[11]  Hadley C. Bergstrom,et al.  Pavlovian Fear Conditioning Activates a Common Pattern of Neurons in the Lateral Amygdala of Individual Brains , 2011, PloS one.

[12]  Serge Laroche,et al.  Reconsolidation of memory: A decade of debate , 2012, Progress in Neurobiology.

[13]  Paul W. Frankland,et al.  Increasing CRTC1 Function in the Dentate Gyrus during Memory Formation or Reactivation Increases Memory Strength without Compromising Memory Quality , 2012, The Journal of Neuroscience.

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

[15]  Emmanuel Roze,et al.  Role of the ERK/MSK1 signalling pathway in chromatin remodelling and brain responses to drugs of abuse , 2009, Journal of neurochemistry.

[16]  Xi Chen,et al.  PI3 kinase signaling is required for retrieval and extinction of contextual memory , 2005, Nature Neuroscience.

[17]  A. Bode,et al.  Inducible Covalent Posttranslational Modification of Histone H3 , 2005, Science's STKE.

[18]  X. Chen,et al.  Hippocampal CRE-mediated gene expression is required for contextual memory formation , 2002, Nature Neuroscience.

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

[20]  George Paxinos,et al.  The Mouse Brain in Stereotaxic Coordinates , 2001 .

[21]  M. Fanselow,et al.  The Amygdala and Fear Conditioning: Has the Nut Been Cracked? , 1996, Neuron.

[22]  J. Sweatt,et al.  A necessity for MAP kinase activation in mammalian spatial learning. , 1999, Learning & memory.

[23]  E. Wagenmakers,et al.  Erroneous analyses of interactions in neuroscience: a problem of significance , 2011, Nature Neuroscience.

[24]  S. Davis,et al.  Distinctive features of Egr transcription factor regulation and DNA binding activity in CA1 of the hippocampus in synaptic plasticity and consolidation and reconsolidation of fear memory , 2012, Hippocampus.

[25]  Anastassios V. Tzingounis,et al.  Arc/Arg3.1: Linking Gene Expression to Synaptic Plasticity and Memory , 2006, Neuron.

[26]  H. Maldonado,et al.  Midazolam disrupts fear memory reconsolidation , 2006, Neuroscience.

[27]  R. Huganir,et al.  MAPK cascade signalling and synaptic plasticity , 2004, Nature Reviews Neuroscience.

[28]  J. Sweatt,et al.  The IκB Kinase Regulates Chromatin Structure during Reconsolidation of Conditioned Fear Memories , 2007, Neuron.

[29]  M. Fendt,et al.  The neuroanatomical and neurochemical basis of conditioned fear , 1999, Neuroscience & Biobehavioral Reviews.

[30]  L. Kaczmarek,et al.  Differential response of two subdivisions of lateral amygdala to aversive conditioning as revealed by c-Fos and P-ERK mapping , 2002, Neuroreport.

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

[32]  Gernot Riedel,et al.  Foreground contextual fear memory consolidation requires two independent phases of hippocampal ERK/CREB activation. , 2006, Learning & memory.

[33]  D. Storm,et al.  Ca2+-Stimulated Adenylyl Cyclases Regulate ERK-Dependent Activation of MSK1 during Fear Conditioning , 2007, Neuron.

[34]  M. Fanselow.  Contextual fear, gestalt memories, and the hippocampus , 2000, Behavioural Brain Research.

[35]  Joseph E LeDoux,et al.  Activation of extracellular signal‐regulated kinase– mitogen‐activated protein kinase cascade in the amygdala is required for memory reconsolidation of auditory fear conditioning , 2005, The European journal of neuroscience.

[36]  G. Quirk,et al.  Neuronal signalling of fear memory , 2004, Nature Reviews Neuroscience.

[37]  N. Mons,et al.  Biphasic ERK1/2 activation in both the hippocampus and amygdala may reveal a system consolidation of contextual fear memory , 2007, Neurobiology of Learning and Memory.

[38]  Joseph E LeDoux,et al.  Lesions of the dorsal hippocampal formation interfere with background but not foreground contextual fear conditioning. , 1994, Learning & memory.

[39]  W. C. Gordon.  Susceptibility of a reactivated memory to the effects of strychnine: A time-dependent phenomenon , 1977, Physiology & Behavior.

[40]  J. Sweatt,et al.  Neuronal MEK is important for normal fear conditioning in mice , 2004, Journal of neuroscience research.

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

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

[43]  M. Besson,et al.  Extracellular Signal-Regulated Kinase (ERK) Controls Immediate Early Gene Induction on Corticostriatal Stimulation , 1998, The Journal of Neuroscience.

[44]  N. Spear,et al.  The effects of strychnine on recently acquired and reactivated passive avoidance memories. , 1973, Physiology & behavior.

[45]  A. Besnard,et al.  A Model of Hippocampal Competition between New Learning and Memory Updating , 2012, The Journal of Neuroscience.

[46]  Joseph E LeDoux,et al.  Activation of ERK/MAP Kinase in the Amygdala Is Required for Memory Consolidation of Pavlovian Fear Conditioning , 2000, The Journal of Neuroscience.

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

[48]  Satoshi Kida,et al.  Brain Region-Specific Gene Expression Activation Required for Reconsolidation and Extinction of Contextual Fear Memory , 2009, The Journal of Neuroscience.

[49]  W. Wurst,et al.  Activation of ERK/MAPK in the Lateral Amygdala of the Mouse is Required for Acquisition of a Fear-Potentiated Startle response , 2009, Neuropsychopharmacology.

[50]  J. David Sweatt,et al.  Epigenetic Mechanisms in Cognition , 2011, Neuron.

[51]  J. Milbrandt,et al.  Structure of the NGFI-A gene and detection of upstream sequences responsible for its transcriptional induction by nerve growth factor. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[52]  B. Hars,et al.  Extracellular signal‐regulated kinase activation is required for consolidation and reconsolidation of memory at an early stage of ontogenesis , 2009, The European journal of neuroscience.

[53]  K. Deisseroth,et al.  Optogenetic stimulation of a hippocampal engram activates fear memory recall , 2012, Nature.

[54]  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.

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

[56]  J. Radulovic,et al.  Phosphorylation of Hippocampal Erk-1/2, Elk-1, and p90-Rsk-1 during Contextual Fear Conditioning: Interactions between Erk-1/2 and Elk-1 , 2002, Molecular and Cellular Neuroscience.

[57]  JaneR . Taylor,et al.  The Striatal-Enriched Protein Tyrosine Phosphatase Gates Long-Term Potentiation and Fear Memory in the Lateral Amygdala , 2007, Biological Psychiatry.

[58]  J. Guzowski,et al.  Using immediate-early genes to map hippocampal subregional functions. , 2007, Learning & memory.

[59]  A. Treves,et al.  Distinct Ensemble Codes in Hippocampal Areas CA3 and CA1 , 2004, Science.

[60]  M. Fanselow,et al.  Conditional and unconditional components of post-shock freezing , 1980, The Pavlovian journal of biological science.

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

[62]  Joseph E LeDoux.  Emotion Circuits in the Brain , 2000 .

[63]  Hyejin Kang,et al.  Translational Control by MAPK Signaling in Long-Term Synaptic Plasticity and Memory , 2004, Cell.

[64]  Alfred Nordheim,et al.  Chromatin structure analysis of the human c-fos promoter reveals a centrally positioned nucleosome , 1997, Chromosoma.

[65]  Joseph E LeDoux,et al.  Disruption of reconsolidation but not consolidation of auditory fear conditioning by noradrenergic blockade in the amygdala , 2004, Neuroscience.