Common molecular mechanisms in explicit and implicit memory

Cellular and molecular studies of both implicit and explicit memory suggest that experience‐dependent modulation of synaptic strength and structure is a fundamental mechanism by which these memories are encoded and stored within the brain. In this review, we focus on recent advances in our understanding of two types of memory storage: (i) sensitization in Aplysia, a simple form of implicit memory, and (ii) formation of explicit spatial memories in the mouse hippocampus. These two processes share common molecular mechanisms that have been highly conserved through evolution.

[1]  Roberto Malinow,et al.  LTP mechanisms: from silence to four-lane traffic , 2000, Current Opinion in Neurobiology.

[2]  Michael A Sutton,et al.  Inhibition of calcineurin facilitates the induction of memory for sensitization in Aplysia: Requirement of mitogen-activated protein kinase , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[3]  E. Villacres,et al.  Induction of CRE-Mediated Gene Expression by Stimuli That Generate Long-Lasting LTP in Area CA1 of the Hippocampus , 1996, Neuron.

[4]  U. Frey,et al.  Synaptic tagging and long-term potentiation , 1997, Nature.

[5]  Wade Morishita,et al.  Generation of Silent Synapses by Acute In Vivo Expression of CaMKIV and CREB , 2005, Neuron.

[6]  Shiu-Hwa Yeh,et al.  Acetylation of nuclear factor-kappaB in rat amygdala improves long-term but not short-term retention of fear memory. , 2004, Molecular pharmacology.

[7]  Y. Jan,et al.  dunce, a mutant of Drosophila deficient in learning. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[8]  E. Kandel,et al.  Genetic and Pharmacological Evidence for a Novel, Intermediate Phase of Long-Term Potentiation Suppressed by Calcineurin , 1998, Cell.

[9]  Eric R Kandel,et al.  CREB1 Encodes a Nuclear Activator, a Repressor, and a Cytoplasmic Modulator that Form a Regulatory Unit Critical for Long-Term Facilitation , 1998, Cell.

[10]  F. Crick Memory and molecular turnover. , 1984, Nature.

[11]  E. Kandel,et al.  Memory suppressor genes: inhibitory constraints on the storage of long-term memory. , 1998, Science.

[12]  Sheena A. Josselyn,et al.  Long-Term Memory Is Facilitated by cAMP Response Element-Binding Protein Overexpression in the Amygdala , 2001, The Journal of Neuroscience.

[13]  Andrew I Su,et al.  Genome-wide analysis of CREB target genes reveals a core promoter requirement for cAMP responsiveness. , 2003, Molecular cell.

[14]  J. Fiala,et al.  Polyribosomes Redistribute from Dendritic Shafts into Spines with Enlarged Synapses during LTP in Developing Rat Hippocampal Slices , 2002, Neuron.

[15]  Eric R. Kandel,et al.  Reversible Inhibition of CREB/ATF Transcription Factors in Region CA1 of the Dorsal Hippocampus Disrupts Hippocampus-Dependent Spatial Memory , 2002, Neuron.

[16]  F. Gage,et al.  Chromatin remodeling in neural development and plasticity. , 2005, Current opinion in cell biology.

[17]  T. Bliss,et al.  A role for dendritic protein synthesis in hippocampal late LTP , 2003, The European journal of neuroscience.

[18]  W. Tischmeyer,et al.  Activation of immediate early genes and memory formation , 1999, Cellular and Molecular Life Sciences CMLS.

[19]  E. Kandel,et al.  Enhancement of Memory-Related Long-Term Facilitation by ApAF, a Novel Transcription Factor that Acts Downstream from Both CREB1 and CREB2 , 2000, Cell.

[20]  E. Kandel,et al.  Cell and molecular analysis of long-term sensitization in Aplysia. , 1986, Journal de physiologie.

[21]  E. Kandel,et al.  Structural changes accompanying memory storage. , 1993, Annual review of physiology.

[22]  D. Storm,et al.  Stimulation of cAMP response element (CRE)-mediated transcription during contextual learning , 1998, Nature Neuroscience.

[23]  K. Deisseroth,et al.  Signaling from Synapse to Nucleus: Postsynaptic CREB Phosphorylation during Multiple Forms of Hippocampal Synaptic Plasticity , 1996, Neuron.

[24]  Ronald L. Davis,et al.  Defect in cyclic AMP phosphodiesterase due to the dunce mutation of learning in Drosophila melanogaster , 1981, Nature.

[25]  D. Linden,et al.  A Late Phase of Cerebellar Long-Term Depression Requires Activation of CaMKIV and CREB , 1999, Neuron.

[26]  T. Tully,et al.  CREB as a Memory Modulator: induced expression of a dCREB2 activator isoform enhances long-term memory in drosophila , 1995, Cell.

[27]  D. Molfese,et al.  Regulation of Histone Acetylation during Memory Formation in the Hippocampus* , 2004, Journal of Biological Chemistry.

[28]  M. Segal Dendritic spines and long-term plasticity , 2005, Nature Reviews Neuroscience.

[29]  Alison L. Barth,et al.  Upregulation of cAMP Response Element-Mediated Gene Expression during Experience-Dependent Plasticity in Adult Neocortex , 2000, The Journal of Neuroscience.

[30]  S. Josselyn,et al.  Inducible repression of CREB function disrupts amygdala-dependent memory , 2004, Neurobiology of Learning and Memory.

[31]  Eric R. Kandel,et al.  Two previously undescribed members of the mouse CPEB family of genes and their inducible expression in the principal cell layers of the hippocampus , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[32]  C. H. Bailey,et al.  Long-term memory in Aplysia modulates the total number of varicosities of single identified sensory neurons. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[33]  L. B. Flexner,et al.  Memory and cerebral protein synthesis in mice as affected by graded amounts of puromycin. , 1965, Experimental neurology.

[34]  C. H. Bailey,et al.  Long-term sensitization in Aplysia increases the number of presynaptic contacts onto the identified gill motor neuron L7. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[35]  W. Schmid,et al.  Targeting of the CREB gene leads to up‐regulation of a novel CREB mRNA isoform. , 1996, The EMBO journal.

[36]  E. Kandel,et al.  Chromatin Acetylation, Memory, and LTP Are Impaired in CBP+/− Mice A Model for the Cognitive Deficit in Rubinstein-Taybi Syndrome and Its Amelioration , 2004, Neuron.

[37]  Thomas Lemberger,et al.  SRF mediates activity-induced gene expression and synaptic plasticity but not neuronal viability , 2005, Nature Neuroscience.

[38]  P. Serrano,et al.  Protein synthesis‐dependent LTP in isolated dendrites of CA1 pyramidal cells , 2005, Hippocampus.

[39]  E. Kandel,et al.  Target-dependent structural changes accompanying long-term synaptic facilitation in Aplysia neurons. , 1990, Science.

[40]  J. David Sweatt,et al.  A Requirement for the Mitogen-activated Protein Kinase Cascade in Hippocampal Long Term Potentiation* , 1997, The Journal of Biological Chemistry.

[41]  E. Kandel,et al.  Serotonin-Induced Regulation of the Actin Network for Learning-Related Synaptic Growth Requires Cdc42, N-WASP, and PAK in Aplysia Sensory Neurons , 2005, Neuron.

[42]  G. Ellis‐Davies,et al.  Structural basis of long-term potentiation in single dendritic spines , 2004, Nature.

[43]  Eric R Kandel,et al.  Capture of the Late Phase of Long-Term Potentiation within and across the Apical and Basilar Dendritic Compartments of CA1 Pyramidal Neurons: Synaptic Tagging Is Compartment Restricted , 2006, The Journal of Neuroscience.

[44]  P. Demoly,et al.  [Transgenic mice]. , 1992, Annales de dermatologie et de venereologie.

[45]  E. Kandel,et al.  Genetic Demonstration of a Role for PKA in the Late Phase of LTP and in Hippocampus-Based Long-Term Memory , 1997, Cell.

[46]  U. Frey,et al.  Deficits in memory tasks of mice with CREB mutations depend on gene dosage. , 1998, Learning & memory.

[47]  Irving Kupfermann,et al.  Neuronal Correlates of Habituation and Dishabituation of the Gill-Withdrawal Reflex in Aplysia , 1970, Science.

[48]  W. Gan,et al.  Development of Long-Term Dendritic Spine Stability in Diverse Regions of Cerebral Cortex , 2005, Neuron.

[49]  E. Kandel,et al.  C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia , 1994, Cell.

[50]  E R Kandel,et al.  Synaptic facilitation and behavioral sensitization in Aplysia: possible role of serotonin and cyclic AMP. , 1976, Science.

[51]  Erin M. Schuman,et al.  Dynamic Visualization of Local Protein Synthesis in Hippocampal Neurons , 2001, Neuron.

[52]  Zhongna Sun,et al.  Presynaptic Morphological Changes Associated with Long-Term Synaptic Facilitation Are Triggered by Actin Polymerization at Preexisting Varicositis , 2000, The Journal of Neuroscience.

[53]  Gero Miesenböck,et al.  Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins , 1998, Nature.

[54]  P. Sanna,et al.  Time-restricted role for dendritic activation of the mTOR-p70S6K pathway in the induction of late-phase long-term potentiation in the CA1 , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[55]  J. David Sweatt,et al.  Epigenetic mechanisms in memory formation , 2005, Nature Reviews Neuroscience.

[56]  P. Tompa,et al.  Prion proteins as memory molecules: an hypothesis. , 1998, Neuroscience.

[57]  E. Kandel,et al.  Synapse-Specific, Long-Term Facilitation of Aplysia Sensory to Motor Synapses: A Function for Local Protein Synthesis in Memory Storage , 1997, Cell.

[58]  Gail Mandel,et al.  Defining the CREB Regulon A Genome-Wide Analysis of Transcription Factor Regulatory Regions , 2004, Cell.

[59]  Yi-shuian Huang,et al.  N‐methyl‐D‐aspartate receptor signaling results in Aurora kinase‐catalyzed CPEB phosphorylation and αCaMKII mRNA polyadenylation at synapses , 2002, The EMBO journal.

[60]  Thomas J. Carew,et al.  Activation of a Tyrosine Kinase-MAPK Cascade Enhances the Induction of Long-Term Synaptic Facilitation and Long-Term Memory in Aplysia , 2003, Neuron.

[61]  C. H. Bailey,et al.  Morphological basis of long-term habituation and sensitization in Aplysia. , 1983, Science.

[62]  Ronald L. Davis,et al.  The Role of cAMP Response Element-Binding Protein in Drosophila Long-Term Memory , 2004, The Journal of Neuroscience.

[63]  W. Quinn,et al.  Three Drosophila mutations that block associative learning also affect habituation and sensitization. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[64]  David P. Wolfer,et al.  Does cAMP Response Element-Binding Protein Have a Pivotal Role in Hippocampal Synaptic Plasticity and Hippocampus-Dependent Memory? , 2003, The Journal of Neuroscience.

[65]  Isabelle M. Mansuy,et al.  Protein phosphatase 1 is a molecular constraint on learning and memory , 2002, Nature.

[66]  F. Crick Neurobiology: Memory and molecular turnover , 1984, Nature.

[67]  E. Kandel,et al.  A Transient, Neuron-Wide Form of CREB-Mediated Long-Term Facilitation Can Be Stabilized at Specific Synapses by Local Protein Synthesis , 1999, Cell.

[68]  W Zieglgänsberger,et al.  Synaptic plasticity in the basolateral amygdala in transgenic mice expressing dominant‐negative cAMP response element‐binding protein (CREB) in forebrain , 2000, The European journal of neuroscience.

[69]  Eric R. Kandel,et al.  Inducible and Reversible Enhancement of Learning, Memory, and Long-Term Potentiation by Genetic Inhibition of Calcineurin , 2001, Cell.

[70]  Joseph E LeDoux,et al.  Structural plasticity and memory , 2004, Nature Reviews Neuroscience.

[71]  E R Kandel,et al.  Serotonin-mediated endocytosis of apCAM: an early step of learning-related synaptic growth in Aplysia. , 1992, Science.

[72]  L. B. Flexner,et al.  INHIBITION OF PROTEIN SYNTHESIS IN BRAIN AND LEARNING AND MEMORY FOLLOWING PUROMYCIN * , 1962, Journal of neurochemistry.

[73]  E. Kandel,et al.  A semi-persistent adult ocular dominance plasticity in visual cortex is stabilized by activated CREB. , 2004, Learning & memory.

[74]  J. David Sweatt,et al.  Activation of p42 Mitogen-activated Protein Kinase in Hippocampal Long Term Potentiation* , 1996, The Journal of Biological Chemistry.

[75]  T. Tully,et al.  A mouse model of Rubinstein-Taybi syndrome: Defective long-term memory is ameliorated by inhibitors of phosphodiesterase 4 , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[76]  E. Kandel,et al.  p38 MAP Kinase Mediates Both Short-Term and Long-Term Synaptic Depression in Aplysia , 2003, The Journal of Neuroscience.

[77]  E R Kandel,et al.  Spatially resolved dynamics of cAMP and protein kinase A subunits in Aplysia sensory neurons. , 1993, Science.

[78]  Alcino J. Silva,et al.  Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein , 1994, Cell.

[79]  E. Kandel,et al.  Role of Aplysia cell adhesion molecules during 5-HT-induced long-term functional and structural changes. , 2003, Learning & memory.

[80]  W. Quinn,et al.  Flies, genes, and learning. , 2001, Annual review of neuroscience.

[81]  E. Kandel,et al.  Inhibitors of protein and RNA synthesis block structural changes that accompany long-term heterosynaptic plasticity in Aplysia , 1992, Neuron.

[82]  D. A. Baxter,et al.  Role of calcium-calmodulin-dependent protein kinase II in modulation of sensorimotor synapses in Aplysia. , 1997, Journal of neurophysiology.

[83]  Eric R Kandel,et al.  MAP Kinase Translocates into the Nucleus of the Presynaptic Cell and Is Required for Long-Term Facilitation in Aplysia , 1997, Neuron.

[84]  Thomas J. Carew,et al.  Molecular Mechanisms Underlying a Unique Intermediate Phase of Memory in Aplysia , 2001, Neuron.

[85]  E. Kandel,et al.  Long-term facilitation in Aplysia involves increase in transmitter release. , 1988, Science.

[86]  U. Frey,et al.  Weak before strong: dissociating synaptic tagging and plasticity-factor accounts of late-LTP , 1998, Neuropharmacology.

[87]  Wolfgang Schmid,et al.  Targeted mutation of the CREB gene: compensation within the CREB/ATF family of transcription factors. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[88]  Dimitris Thanos,et al.  Integration of Long-Term-Memory-Related Synaptic Plasticity Involves Bidirectional Regulation of Gene Expression and Chromatin Structure , 2002, Cell.

[89]  E. Kandel,et al.  A form of long-lasting, learning-related synaptic plasticity in the hippocampus induced by heterosynaptic low-frequency pairing. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[90]  Eric R. Kandel,et al.  Expression of Constitutively Active CREB Protein Facilitates the Late Phase of Long-Term Potentiation by Enhancing Synaptic Capture , 2002, Cell.

[91]  J. Lisman,et al.  A Model of Synaptic Memory A CaMKII/PP1 Switch that Potentiates Transmission by Organizing an AMPA Receptor Anchoring Assembly , 2001, Neuron.

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

[93]  S. J. Martin,et al.  Synaptic plasticity and memory: an evaluation of the hypothesis. , 2000, Annual review of neuroscience.

[94]  E R Kandel,et al.  A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. , 1986, Science.

[95]  D. Ginty,et al.  Function and Regulation of CREB Family Transcription Factors in the Nervous System , 2002, Neuron.

[96]  E. Kandel,et al.  Some Forms of cAMP-Mediated Long-Lasting Potentiation Are Associated with Release of BDNF and Nuclear Translocation of Phospho-MAP Kinase , 2001, Neuron.

[97]  S. Dudek,et al.  Somatic action potentials are sufficient for late-phase LTP-related cell signaling , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[98]  M. Kennedy,et al.  Tetanic Stimulation Leads to Increased Accumulation of Ca2+/Calmodulin-Dependent Protein Kinase II via Dendritic Protein Synthesis in Hippocampal Neurons , 1999, The Journal of Neuroscience.

[99]  K. Deisseroth,et al.  CREB Phosphorylation and Dephosphorylation: A Ca2+- and Stimulus Duration–Dependent Switch for Hippocampal Gene Expression , 1996, Cell.

[100]  Eric R. Kandel,et al.  Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation , 1990, Nature.

[101]  R. Malenka,et al.  AMPA receptor trafficking and synaptic plasticity. , 2002, Annual review of neuroscience.

[102]  Marcelo A Wood,et al.  Transgenic mice expressing a truncated form of CREB-binding protein (CBP) exhibit deficits in hippocampal synaptic plasticity and memory storage. , 2005, Learning & memory.

[103]  I. Lucki,et al.  Behavioral analysis of CREB alphadelta mutation on a B6/129 F1 hybrid background. , 2002, Hippocampus.

[104]  E. Kandel,et al.  Transient expansion of synaptically connected dendritic spines upon induction of hippocampal long-term potentiation. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

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

[106]  E. Kandel,et al.  A Neuronal Isoform of the Aplysia CPEB Has Prion-Like Properties , 2003, Cell.

[107]  M. Bear,et al.  LTP and LTD An Embarrassment of Riches , 2004, Neuron.

[108]  Richard G. Jenner,et al.  Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[109]  Mu-ming Poo,et al.  Shrinkage of Dendritic Spines Associated with Long-Term Depression of Hippocampal Synapses , 2004, Neuron.

[110]  James H. Schwartz,et al.  Ubiquitin C-Terminal Hydrolase Is an Immediate-Early Gene Essential for Long-Term Facilitation in Aplysia , 1997, Cell.

[111]  M. Bear,et al.  Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity , 2000, Nature.

[112]  E. Kandel,et al.  CREB, memory enhancement and the treatment of memory disorders: promises, pitfalls and prospects , 2003, Expert opinion on therapeutic targets.

[113]  W. Quinn,et al.  Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila , 1994, Cell.

[114]  Marc Montminy,et al.  Transcriptional regulation by the phosphorylation-dependent factor CREB , 2001, Nature Reviews Molecular Cell Biology.

[115]  J. Lisman,et al.  The molecular basis of CaMKII function in synaptic and behavioural memory , 2002, Nature Reviews Neuroscience.

[116]  E. Schuman,et al.  Local translational control in dendrites and its role in long-term synaptic plasticity. , 2005, Journal of neurobiology.

[117]  D. Glanzman,et al.  Synaptic Facilitation and Behavioral Dishabituation in Aplysia: Dependence on Release of Ca2+ from Postsynaptic Intracellular Stores, Postsynaptic Exocytosis, and Modulation of Postsynaptic AMPA Receptor Efficacy , 2005, The Journal of Neuroscience.

[118]  INTERNATIONAL SOCIETY FOR NEUROCHEMISTRY , 1976 .

[119]  J. O'Keefe,et al.  The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. , 1971, Brain research.

[120]  O. Steward,et al.  Protein synthesis at synaptic sites on dendrites. , 2001, Annual review of neuroscience.

[121]  T. Bliss,et al.  Long‐lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path , 1973, The Journal of physiology.

[122]  K. Martin,et al.  Synapse to Nucleus Signaling during Long-Term Synaptic Plasticity a Role for the Classical Active Nuclear Import Pathway , 2004, Neuron.

[123]  Mary Chen,et al.  Aplysia CREB2 represses long-term facilitation: Relief of repression converts transient facilitation into long-term functional and structural change , 1995, Cell.

[124]  M. Bear,et al.  A molecular correlate of memory and amnesia in the hippocampus , 1999, Nature Neuroscience.

[125]  E R Kandel,et al.  Serotonin modulates a specific potassium current in the sensory neurons that show presynaptic facilitation in Aplysia. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[126]  M. Mattson,et al.  Evidence for the involvement of TNF and NF‐κB in hippocampal synaptic plasticity , 2000, Synapse.

[127]  Eric R. Kandel,et al.  A Neuronal Isoform of CPEB Regulates Local Protein Synthesis and Stabilizes Synapse-Specific Long-Term Facilitation in Aplysia , 2003, Cell.

[128]  M. Ramaswami Faculty Opinions recommendation of p38 MAP kinase mediates both short-term and long-term synaptic depression in aplysia. , 2003 .

[129]  E. Kandel,et al.  Mutation in the Phosphorylation Sites of MAP Kinase Blocks Learning-Related Internalization of apCAM in Aplysia Sensory Neurons , 1997, Neuron.

[130]  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.

[131]  Eric R Kandel,et al.  A novel intermediate stage in the transition between short- and long-term facilitation in the sensory to motor neuron synapse of aplysia , 1995, Neuron.

[132]  E. Kandel,et al.  Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. , 1993, Science.

[133]  M. Mayford,et al.  CBP Histone Acetyltransferase Activity Is a Critical Component of Memory Consolidation , 2004, Neuron.

[134]  Bernardo L Sabatini,et al.  Neuronal Activity Regulates Diffusion Across the Neck of Dendritic Spines , 2005, Science.

[135]  Zif and the Survival of Memory , 2004, Science.

[136]  Eric R Kandel,et al.  Restricted and Regulated Overexpression Reveals Calcineurin as a Key Component in the Transition from Short-Term to Long-Term Memory , 1998, Cell.

[137]  R. Malinow,et al.  Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. , 2000, Science.

[138]  S. Barondes,et al.  THE INFLUENCE OF ACTINOMYCIN‐D ON BRAIN RNA SYNTHESIS AND ON MEMORY * , 1964, Journal of neurochemistry.

[139]  Yasunori Hayashi,et al.  Dendritic Spine Geometry: Functional Implication and Regulation , 2005, Neuron.

[140]  E. Kandel,et al.  Modulation of an NCAM-related adhesion molecule with long-term synaptic plasticity in Aplysia. , 1992, Science.

[141]  R. Iyengar,et al.  Postsynaptic CAMP pathway gates early LTP in hippocampal CA1 region , 1995, Neuron.

[142]  Massimo Pandolfo,et al.  Molecular Basis , 2022 .

[143]  E R Kandel,et al.  Neuronal Mechanisms of Habituation and Dishabituation of the Gill-Withdrawal Reflex in Aplysia , 1970, Science.

[144]  M. Waxham,et al.  In situ hybridization histochemistry of Ca2+/calmodulin-dependent protein kinase in developing rat brain , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[145]  E. Kandel,et al.  The Persistence of Long-Term Memory A Molecular Approach to Self-Sustaining Changes in Learning-Induced Synaptic Growth , 2004, Neuron.

[146]  O. Steward,et al.  Compartmentalized Synthesis and Degradation of Proteins in Neurons , 2003, Neuron.

[147]  E. Kandel,et al.  Nitric Oxide Signaling Contributes to Late-Phase LTP and CREB Phosphorylation in the Hippocampus , 1999, The Journal of Neuroscience.

[148]  Ted Abel,et al.  Behavioral analysis of CREB αΔ mutation on a B6/129 F1 hybrid background , 2002 .

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

[150]  Mary Chen,et al.  Presynaptic Activation of Silent Synapses and Growth of New Synapses Contribute to Intermediate and Long-Term Facilitation in Aplysia , 2003, Neuron.

[151]  T. Carew,et al.  Dynamics of Induction and Expression of Long-Term Synaptic Facilitation in Aplysia , 1996, The Journal of Neuroscience.

[152]  Mark Gerstein,et al.  CREB Binds to Multiple Loci on Human Chromosome 22 , 2004, Molecular and Cellular Biology.

[153]  C. H. Bailey,et al.  Structural plasticity at identified synapses during long-term memory in Aplysia. , 1989, Journal of neurobiology.

[154]  T. Bonhoeffer,et al.  Bidirectional Activity-Dependent Morphological Plasticity in Hippocampal Neurons , 2004, Neuron.