Balancing structure and function at hippocampal dendritic spines.

Dendritic spines are the primary recipients of excitatory input in the central nervous system. They provide biochemical compartments that locally control the signaling mechanisms at individual synapses. Hippocampal spines show structural plasticity as the basis for the physiological changes in synaptic efficacy that underlie learning and memory. Spine structure is regulated by molecular mechanisms that are fine-tuned and adjusted according to developmental age, level and direction of synaptic activity, specific brain region, and exact behavioral or experimental conditions. Reciprocal changes between the structure and function of spines impact both local and global integration of signals within dendrites. Advances in imaging and computing technologies may provide the resources needed to reconstruct entire neural circuits. Key to this endeavor is having sufficient resolution to determine the extrinsic factors (such as perisynaptic astroglia) and the intrinsic factors (such as core subcellular organelles) that are required to build and maintain synapses.

[1]  R. L. Singhal,et al.  Glyceraldehyde-3-phosphate dehydrogenase activity in developing brain during experimental cretinism. , 1972, Biochimica et biophysica acta.

[2]  E. Fifková,et al.  Swelling of dendritic spines in the fascia dentata after stimulation of the perforant fibers as a mechanism of post-tetanic potentiation , 1975, Experimental Neurology.

[3]  S. Young,et al.  Effect of anisomycin on stimulation-induced changes in dendritic spines of the dentate granule cells , 1982, Journal of neurocytology.

[4]  W. Levy,et al.  Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  M K Bennett,et al.  Biochemical and immunochemical evidence that the "major postsynaptic density protein" is a subunit of a calmodulin-dependent protein kinase. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[6]  M. Kennedy,et al.  Regulation of brain Type II Ca 2+ calmodulin -dependent protein kinase by autophosphorylation: A Ca2+-triggered molecular switch , 1986, Cell.

[7]  P. Landfield,et al.  Synaptic vesicle redistribution during hippocampal frequency potentiation and depression in young and aged rats , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  O. Steward,et al.  Protein-synthetic machinery beneath postsynaptic sites on CNS neurons: association between polyribosomes and other organelles at the synaptic site , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  K. Harris,et al.  Dendritic spines of rat cerebellar Purkinje cells: serial electron microscopy with reference to their biophysical characteristics , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  KM Harris,et al.  Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  M. Kennedy,et al.  Structure and regulation of type II calcium/calmodulin-dependent protein kinase in central nervous system neurons. , 1990, Cold Spring Harbor symposia on quantitative biology.

[12]  M. Krug,et al.  Spinules in axospinous synapses of the rat dentate gyrus: changes in density following long-term potentiation , 1990, Brain Research.

[13]  Leyla deToledo-Morrell,et al.  Induction of long-term potentiation is associated with an increase in the number of axospinous synapses with segmented postsynaptic densities , 1991, Brain Research.

[14]  V. Popov,et al.  Hibernation-induced structural changes in synaptic contacts between mossy fibres and hippocampal pyramidal neurons , 1992, Neuroscience.

[15]  K M Harris,et al.  Three‐dimensional analysis of the structure and composition of CA3 branched dendritic spines and their synaptic relationships with mossy fiber boutons in the rat hippocampus , 1992, The Journal of comparative neurology.

[16]  K. Harris,et al.  Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  A. Bragin,et al.  Repeated changes of dendritic morphology in the hippocampus of ground squirrels in the course of hibernation , 1992, Neuroscience.

[18]  Kristen M. Harris,et al.  Quantal analysis and synaptic anatomy — integrating two views of hippocampal plasticity , 1993, Trends in Neurosciences.

[19]  F. Morrell,et al.  Structural synaptic correlate of long‐term potentiation: Formation of axospinous synapses with multiple, completely partitioned transmission zones , 1993, Hippocampus.

[20]  T. Soderling,et al.  Phosphorylation and regulation of glutamate receptors by calcium/calmodulin-dependent protein kinase II , 1993, Nature.

[21]  R. Malinow,et al.  Potentiated transmission and prevention of further LTP by increased CaMKII activity in postsynaptic hippocampal slice neurons. , 1994, Science.

[22]  J. Lisman,et al.  Who's been nibbling on my PSD: Is it LTD? , 1994, Journal of Physiology-Paris.

[23]  J. Isaac,et al.  Evidence for silent synapses: Implications for the expression of LTP , 1995, Neuron.

[24]  R. Malinow,et al.  Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice , 1995, Nature.

[25]  R. Nicoll,et al.  Calcium/calmodulin-dependent kinase II and long-term potentiation enhance synaptic transmission by the same mechanism. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[26]  M. Segal,et al.  Morphological plasticity in dendritic spines of cultured hippocampal neurons , 1996, Neuroscience.

[27]  Mark Ellisman,et al.  Ultrastructural Localization of Dendritic Messenger RNA in Adult Rat Hippocampus , 1996, The Journal of Neuroscience.

[28]  P. Andersen,et al.  Long-term potentiation is associated with new excitatory spine synapses on rat dentate granule cells. , 1996, Learning & memory.

[29]  Stephen J. Smith,et al.  Evidence for a Role of Dendritic Filopodia in Synaptogenesis and Spine Formation , 1996, Neuron.

[30]  I. Weiler,et al.  Fragile X mental retardation protein is translated near synapses in response to neurotransmitter activation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[31]  P. Andersen,et al.  Spatial training in a complex environment and isolation alter the spine distribution differently in rat CA1 pyramidal cells. , 1997, The Journal of comparative neurology.

[32]  K M Harris,et al.  Visualization of the Distribution of Autophosphorylated Calcium/Calmodulin-Dependent Protein Kinase II after Tetanic Stimulation in the CA1 Area of the Hippocampus , 1997, The Journal of Neuroscience.

[33]  P Siekevitz,et al.  The synthesis of ATP by glycolytic enzymes in the postsynaptic density and the effect of endogenously generated nitric oxide. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Ann Marie Craig,et al.  Activity Regulates the Synaptic Localization of the NMDA Receptor in Hippocampal Neurons , 1997, Neuron.

[35]  K M Harris,et al.  Three-Dimensional Organization of Smooth Endoplasmic Reticulum in Hippocampal CA1 Dendrites and Dendritic Spines of the Immature and Mature Rat , 1997, The Journal of Neuroscience.

[36]  M. Kennedy,et al.  A Synaptic Ras-GTPase Activating Protein (p135 SynGAP) Inhibited by CaM Kinase II , 1998, Neuron.

[37]  J. Fiala,et al.  Synaptogenesis Via Dendritic Filopodia in Developing Hippocampal Area CA1 , 1998, The Journal of Neuroscience.

[38]  R. Huganir,et al.  SynGAP: a Synaptic RasGAP that Associates with the PSD-95/SAP90 Protein Family , 1998, Neuron.

[39]  S. Halpain,et al.  Regulation of F-Actin Stability in Dendritic Spines by Glutamate Receptors and Calcineurin , 1998, The Journal of Neuroscience.

[40]  J. Fiala,et al.  Critical assessment of the involvement of perforations, spinules, and spine branching in hippocampal synapse formation , 1998, The Journal of comparative neurology.

[41]  K. Svoboda,et al.  Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. , 1999, Science.

[42]  Richard L. Huganir,et al.  Regulation of morphological postsynaptic silent synapses in developing hippocampal neurons , 1999, Nature Neuroscience.

[43]  K. Harris,et al.  Dendrites are more spiny on mature hippocampal neurons when synapses are inactivated , 1999, Nature Neuroscience.

[44]  Richard D. Fetter,et al.  Watching a Synapse Grow Noninvasive Confocal Imaging of Synaptic Growth in Drosophila , 1999, Neuron.

[45]  O. Ottersen,et al.  The Arrangement of Glutamate Receptors in Excitatory Synapses , 1999, Annals of the New York Academy of Sciences.

[46]  Petter Laake,et al.  Different modes of expression of AMPA and NMDA receptors in hippocampal synapses , 1999, Nature Neuroscience.

[47]  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.

[48]  John E. Lisman,et al.  A Role of Actin Filament in Synaptic Transmission and Long-Term Potentiation , 1999, The Journal of Neuroscience.

[49]  A. Triller,et al.  Dendritic and Postsynaptic Protein Synthetic Machinery , 1999, The Journal of Neuroscience.

[50]  F. Engert,et al.  Dendritic spine changes associated with hippocampal long-term synaptic plasticity , 1999, Nature.

[51]  K. Harris,et al.  Slices Have More Synapses than Perfusion-Fixed Hippocampus from both Young and Mature Rats , 1999, The Journal of Neuroscience.

[52]  J. Partridge,et al.  Selective acquisition of AMPA receptors over postnatal development suggests a molecular basis for silent synapses , 1999, Nature Neuroscience.

[53]  Kristen M Harris,et al.  Structure, development, and plasticity of dendritic spines , 1999, Current Opinion in Neurobiology.

[54]  N. Toni,et al.  LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite , 1999, Nature.

[55]  K. Harris,et al.  Three-Dimensional Relationships between Hippocampal Synapses and Astrocytes , 1999, The Journal of Neuroscience.

[56]  M. Fischer,et al.  Glutamate receptors regulate actin-based plasticity in dendritic spines , 2000, Nature Neuroscience.

[57]  L. Cramer Myosin VI , 2000, The Journal of cell biology.

[58]  Michael E Greenberg,et al.  EphB Receptors Interact with NMDA Receptors and Regulate Excitatory Synapse Formation , 2000, Cell.

[59]  P. Crino,et al.  Stimulation of glutamate receptor protein synthesis and membrane insertion within isolated neuronal dendrites. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[60]  S. Halpain,et al.  Dynamic actin filaments are required for stable long-term potentiation (LTP) in area CA1 of the hippocampus. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[61]  J. D. McGaugh,et al.  Translocation machinery for synthesis of integral membrane and secretory proteins in dendritic spines , 2000, Nature Neuroscience.

[62]  O. Bozdagi,et al.  Increasing Numbers of Synaptic Puncta during Late-Phase LTP N-Cadherin Is Synthesized, Recruited to Synaptic Sites, and Required for Potentiation , 2000, Neuron.

[63]  Yu Tian Wang,et al.  Regulation of AMPA Receptor–Mediated Synaptic Transmission by Clathrin-Dependent Receptor Internalization , 2000, Neuron.

[64]  A. Matus,et al.  Actin-based plasticity in dendritic spines. , 2000, Science.

[65]  Mark von Zastrow,et al.  Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD , 2000, Nature Neuroscience.

[66]  G. Marrs,et al.  Rapid formation and remodeling of postsynaptic densities in developing dendrites , 2001, Nature Neuroscience.

[67]  M. Goldberg,et al.  Dendritic Spines Lost during Glutamate Receptor Activation Reemerge at Original Sites of Synaptic Contact , 2001, The Journal of Neuroscience.

[68]  K. Svoboda,et al.  Ca2+ signaling in dendritic spines , 2001, Current Opinion in Neurobiology.

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

[70]  M. Bear,et al.  Chemical induction of mGluR5- and protein synthesis--dependent long-term depression in hippocampal area CA1. , 2001, Journal of neurophysiology.

[71]  松崎 政紀 Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons , 2001 .

[72]  Eckart D. Gundelfinger,et al.  Assembling the Presynaptic Active Zone A Characterization of an Active Zone Precursor Vesicle , 2001, Neuron.

[73]  Wei-Yang Lu,et al.  Activation of Synaptic NMDA Receptors Induces Membrane Insertion of New AMPA Receptors and LTP in Cultured Hippocampal Neurons , 2001, Neuron.

[74]  H. Okado,et al.  Spine Formation and Correlated Assembly of Presynaptic and Postsynaptic Molecules , 2001, The Journal of Neuroscience.

[75]  Mark F. Bear,et al.  Internalization of ionotropic glutamate receptors in response to mGluR activation , 2001, Nature Neuroscience.

[76]  Roger A. Nicoll,et al.  Metabotropic glutamate receptor activation causes a rapid redistribution of AMPA receptors , 2001, Neuropharmacology.

[77]  S. Heinemann,et al.  Trans-Synaptic Eph Receptor-Ephrin Signaling in Hippocampal Mossy Fiber LTP , 2002, Science.

[78]  Venkatesh N. Murthy,et al.  Rapid turnover of actin in dendritic spines and its regulation by activity , 2002, Nature Neuroscience.

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

[80]  R. Malinow,et al.  Ras and Rap Control AMPA Receptor Trafficking during Synaptic Plasticity , 2002, Cell.

[81]  M. Takeichi,et al.  Cadherin Regulates Dendritic Spine Morphogenesis , 2002, Neuron.

[82]  M. Ehlers,et al.  Dynamics and Regulation of Clathrin Coats at Specialized Endocytic Zones of Dendrites and Spines , 2002, Neuron.

[83]  J. Fiala,et al.  Dendritic spines do not split during hippocampal LTP or maturation , 2002, Nature Neuroscience.

[84]  Yu Tian Wang,et al.  Clathrin Adaptor AP2 and NSF Interact with Overlapping Sites of GluR2 and Play Distinct Roles in AMPA Receptor Trafficking and Hippocampal LTD , 2002, Neuron.

[85]  J. Fiala,et al.  Endosomal Compartments Serve Multiple Hippocampal Dendritic Spines from a Widespread Rather Than a Local Store of Recycling Membrane , 2002, The Journal of Neuroscience.

[86]  Mark Ellisman,et al.  Protoplasmic Astrocytes in CA1 Stratum Radiatum Occupy Separate Anatomical Domains , 2002, The Journal of Neuroscience.

[87]  K. Murai,et al.  Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling , 2003, Nature Neuroscience.

[88]  C. Bramham,et al.  Bursts of high‐frequency stimulation trigger rapid delivery of pre‐existing α‐CaMKII mRNA to synapses: a mechanism in dendritic protein synthesis during long‐term potentiation in adult awake rats , 2003, The European journal of neuroscience.

[89]  R. Huganir,et al.  Rapid Induction of Dendritic Spine Morphogenesis by trans-Synaptic EphrinB-EphB Receptor Activation of the Rho-GEF Kalirin , 2003, Neuron.

[90]  N. Ziv,et al.  Unitary Assembly of Presynaptic Active Zones from Piccolo-Bassoon Transport Vesicles , 2003, Neuron.

[91]  Yasuhiko Ohta,et al.  Hippocampal LTP Is Accompanied by Enhanced F-Actin Content within the Dendritic Spine that Is Essential for Late LTP Maintenance In Vivo , 2003, Neuron.

[92]  A. Matus,et al.  Activity-induced targeting of profilin and stabilization of dendritic spine morphology , 2003, Nature Neuroscience.

[93]  Kristen M Harris,et al.  Structural changes at dendritic spine synapses during long-term potentiation. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[95]  John Lisman,et al.  Persistent Accumulation of Calcium/Calmodulin-Dependent Protein Kinase II in Dendritic Spines after Induction of NMDA Receptor-Dependent Chemical Long-Term Potentiation , 2004, The Journal of Neuroscience.

[96]  Mikyoung Park,et al.  Recycling Endosomes Supply AMPA Receptors for LTP , 2004, Science.

[97]  Karel Svoboda,et al.  Induction of Spine Growth and Synapse Formation by Regulation of the Spine Actin Cytoskeleton , 2004, Neuron.

[98]  M. Lynch,et al.  Expression of long‐term potentiation in aged rats involves perforated synapses but dendritic spine branching results from high‐frequency stimulation alone , 2004, Hippocampus.

[99]  K. Harris,et al.  Trans-Endocytosis via Spinules in Adult Rat Hippocampus , 2004, The Journal of Neuroscience.

[100]  R. Cohen,et al.  Glyceraldehyde-3-Phosphate Dehydrogenase Activity and F-Actin Associations in Synaptosomes and Postsynaptic Densities of Porcine Cerebral Cortex , 1997, Cellular and Molecular Neurobiology.

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

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

[103]  J. Fiala,et al.  Dendritic spines disappear with chilling but proliferate excessively upon rewarming of mature hippocampus , 2004, Neuroscience.

[104]  M. Kennedy,et al.  SynGAP Regulates Spine Formation , 2004, The Journal of Neuroscience.

[105]  V. Doyère,et al.  Long‐term synaptic morphometry changes after induction of long‐term potentiation and long‐term depression in the dentate gyrus of awake rats are not simply mirror phenomena , 2004, The European journal of neuroscience.

[106]  B. Barres,et al.  Role for glia in synaptogenesis , 2004, Glia.

[107]  M. Frotscher,et al.  Hippocampal plasticity requires postsynaptic ephrinBs , 2004, Nature Neuroscience.

[108]  J. Špaček,et al.  Three-dimensional analysis of dendritic spines , 2004, Anatomy and Embryology.

[109]  K. Harris,et al.  Age-dependence in the homeostatic upregulation of hippocampal dendritic spine number during blocked synaptic transmission , 2004, Neuropharmacology.

[110]  M. Ehlers,et al.  Secretory trafficking in neuronal dendrites , 2004, Nature Cell Biology.

[111]  M. Kennedy,et al.  Regulation of the Neuron-specific Ras GTPase-activating Protein, synGAP, by Ca2+/Calmodulin-dependent Protein Kinase II* , 2004, Journal of Biological Chemistry.

[112]  M. Ehlers,et al.  Lateral organization of endocytic machinery in dendritic spines , 2004, Nature Neuroscience.

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

[114]  Yasunori Hayashi,et al.  The Importance of Dendritic Mitochondria in the Morphogenesis and Plasticity of Spines and Synapses , 2004, Cell.

[115]  M. Takeichi,et al.  Stability of dendritic spines and synaptic contacts is controlled by αN-catenin , 2004, Nature Neuroscience.

[116]  R. Tsien,et al.  Activity-dependent regulation of dendritic synthesis and trafficking of AMPA receptors , 2004, Nature Neuroscience.

[117]  T. Bliss,et al.  Remodelling of synaptic morphology but unchanged synaptic density during late phase long-term potentiation(ltp): A serial section electron micrograph study in the dentate gyrus in the anaesthetised rat , 2004, Neuroscience.

[118]  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.

[119]  F. Irie,et al.  EPHB receptor signaling in dendritic spine development. , 2004, Frontiers in bioscience : a journal and virtual library.

[120]  D. Clapham,et al.  SynGAP-MUPP1-CaMKII Synaptic Complexes Regulate p38 MAP Kinase Activity and NMDA Receptor- Dependent Synaptic AMPA Receptor Potentiation , 2004, Neuron.

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

[122]  J. Špaček,et al.  Three-Dimensional analysis of dendritic spines , 1983, Anatomy and Embryology.

[123]  J. Bourne,et al.  The role of actin in the regulation of dendritic spine morphology and bidirectional synaptic plasticity , 2004, Neuroreport.

[124]  K. Kosik,et al.  Delta-catenin at the synaptic-adherens junction. , 2005, Trends in cell biology.

[125]  B. Barres,et al.  Signaling between glia and neurons: focus on synaptic plasticity , 2005, Current Opinion in Neurobiology.

[126]  S. Grant,et al.  Dynamic distribution of endoplasmic reticulum in hippocampal neuron dendritic spines , 2005, The European journal of neuroscience.

[127]  K. Murphy,et al.  Chemically induced long‐term potentiation increases the number of perforated and complex postsynaptic densities but does not alter dendritic spine volume in CA1 of adult mouse hippocampal slices , 2005, The European journal of neuroscience.

[128]  T. Oertner,et al.  Calcium regulation of actin dynamics in dendritic spines. , 2005, Cell calcium.

[129]  Hillel Adesnik,et al.  Photoinactivation of Native AMPA Receptors Reveals Their Real-Time Trafficking , 2005, Neuron.

[130]  K. M. Huber,et al.  Developmental Switch in Synaptic Mechanisms of Hippocampal Metabotropic Glutamate Receptor-Dependent Long-Term Depression , 2005, The Journal of Neuroscience.

[131]  A. VanDongen,et al.  Translation of an integral membrane protein in distal dendrites of hippocampal neurons , 2005, The European journal of neuroscience.

[132]  P. Strata,et al.  Axonal and synaptic remodeling in the mature cerebellar cortex. , 2005, Progress in brain research.

[133]  K. Kosik,et al.  δ-Catenin at the synaptic–adherens junction , 2005 .

[134]  Maryann E Martone,et al.  Transient decrease in F‐actin may be necessary for translocation of proteins into dendritic spines , 2005, The European journal of neuroscience.

[135]  Andreas Lüthi,et al.  Dendritic Spine Heterogeneity Determines Afferent-Specific Hebbian Plasticity in the Amygdala , 2005, Neuron.

[136]  J. Hell,et al.  Thrombospondins Are Astrocyte-Secreted Proteins that Promote CNS Synaptogenesis , 2005, Cell.

[137]  Richard L. Huganir,et al.  Activity-Dependent Dendritic Spine Structural Plasticity Is Regulated by Small GTPase Rap1 and Its Target AF-6 , 2005, Neuron.

[138]  J. Esteban,et al.  NMDA Receptor-Dependent Activation of the Small GTPase Rab5 Drives the Removal of Synaptic AMPA Receptors during Hippocampal LTD , 2005, Neuron.

[139]  M. Mooseker,et al.  A role for myosin VI in postsynaptic structure and glutamate receptor endocytosis , 2005, The Journal of cell biology.

[140]  Elena B. Pasquale,et al.  Molecular mechanisms of dendritic spine development and remodeling , 2005, Progress in Neurobiology.

[141]  Daniel Johnston,et al.  Plasticity of dendritic function , 2005, Current Opinion in Neurobiology.

[142]  Gary Lynch,et al.  Theta Stimulation Polymerizes Actin in Dendritic Spines of Hippocampus , 2005, The Journal of Neuroscience.

[143]  Yevgenia Kozorovitskiy,et al.  Experience induces structural and biochemical changes in the adult primate brain. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[144]  Nelson Spruston,et al.  Distance-Dependent Differences in Synapse Number and AMPA Receptor Expression in Hippocampal CA1 Pyramidal Neurons , 2006, Neuron.

[145]  K. Mori,et al.  Telencephalin Slows Spine Maturation , 2006, The Journal of Neuroscience.

[146]  T. Knöpfel,et al.  Involvement of Protein Synthesis and Degradation in Long-Term Potentiation of Schaffer Collateral CA1 Synapses , 2006, The Journal of Neuroscience.

[147]  R. Weinberg,et al.  A Critical Role for Myosin IIB in Dendritic Spine Morphology and Synaptic Function , 2006, Neuron.

[148]  J. Henley,et al.  Lateral Diffusion Drives Constitutive Exchange of AMPA Receptors at Dendritic Spines and Is Regulated by Spine Morphology , 2006, The Journal of Neuroscience.

[149]  J. Bourne,et al.  Uniform Serial Sectioning for Transmission Electron Microscopy , 2006, The Journal of Neuroscience.

[150]  Kristen M. Harris,et al.  Plasticity-Induced Growth of Dendritic Spines by Exocytic Trafficking from Recycling Endosomes , 2006, Neuron.

[151]  R. Huganir,et al.  Regulation of AMPA receptor trafficking by N‐cadherin , 2006, Journal of neurochemistry.

[152]  T. Bonhoeffer,et al.  A Balance of Protein Synthesis and Proteasome-Dependent Degradation Determines the Maintenance of LTP , 2006, Neuron.

[153]  E. Réal,et al.  Analysis of synaptic ultrastructure without fixative using high‐pressure freezing and tomography , 2006, The European journal of neuroscience.

[154]  R. Carroll,et al.  Activity Bidirectionally Regulates AMPA Receptor mRNA Abundance in Dendrites of Hippocampal Neurons , 2006, The Journal of Neuroscience.

[155]  M. Sheng,et al.  Molecular mechanisms of dendritic spine morphogenesis , 2006, Current Opinion in Neurobiology.

[156]  K. Svoboda,et al.  Spine growth precedes synapse formation in the adult neocortex in vivo , 2006, Nature Neuroscience.

[157]  Michael E. Greenberg,et al.  A brain-specific microRNA regulates dendritic spine development , 2006, Nature.

[158]  Barbara Calabrese,et al.  Development and regulation of dendritic spine synapses. , 2006, Physiology.

[159]  Roberto Malinow,et al.  Glutamate Receptor Exocytosis and Spine Enlargement during Chemically Induced Long-Term Potentiation , 2006, The Journal of Neuroscience.

[160]  Michael M. Halassa,et al.  Synaptic Islands Defined by the Territory of a Single Astrocyte , 2007, The Journal of Neuroscience.

[161]  J. Bourne,et al.  Do thin spines learn to be mushroom spines that remember? , 2007, Current Opinion in Neurobiology.

[162]  E. Schuman,et al.  Activity-Regulated N-Cadherin Endocytosis , 2007, Neuron.

[163]  Kevan A. C. Martin,et al.  Protracted Synaptogenesis after Activity-Dependent Spinogenesis in Hippocampal Neurons , 2007, The Journal of Neuroscience.

[164]  B. Sabatini,et al.  Distinct Structural and Ionotropic Roles of NMDA Receptors in Controlling Spine and Synapse Stability , 2007, The Journal of Neuroscience.

[165]  Gary Lynch,et al.  Changes in Synaptic Morphology Accompany Actin Signaling during LTP , 2007, The Journal of Neuroscience.

[166]  Bernardo L Sabatini,et al.  Anatomical and physiological plasticity of dendritic spines. , 2007, Annual review of neuroscience.

[167]  Jeff W Lichtman,et al.  The rise of the 'projectome' , 2007, Nature Methods.

[168]  Shigeo Okabe,et al.  Molecular anatomy of the postsynaptic density , 2007, Molecular and Cellular Neuroscience.

[169]  Kristen M. Harris,et al.  Warmer preparation of hippocampal slices prevents synapse proliferation that might obscure LTP-related structural plasticity , 2007, Neuropharmacology.

[170]  R. Malinow,et al.  PSD-95 is required for activity-driven synapse stabilization , 2007, Proceedings of the National Academy of Sciences.

[171]  Danielle A. Simmons,et al.  Evidence That Long-Term Potentiation Occurs within Individual Hippocampal Synapses during Learning , 2007, The Journal of Neuroscience.

[172]  M. Frotscher,et al.  A role for synaptopodin and the spine apparatus in hippocampal synaptic plasticity. , 2007, Annals of anatomy = Anatomischer Anzeiger : official organ of the Anatomische Gesellschaft.

[173]  R. Shigemoto,et al.  High-resolution quantitative visualization of glutamate and GABA receptors at central synapses , 2007, Current Opinion in Neurobiology.

[174]  J. Bourne,et al.  Polyribosomes are increased in spines of CA1 dendrites 2 h after the induction of LTP in mature rat hippocampal slices , 2007, Hippocampus.

[175]  Sung-Cherl Jung,et al.  Regulation of Dendritic Excitability by Activity-Dependent Trafficking of the A-Type K+ Channel Subunit Kv4.2 in Hippocampal Neurons , 2007, Neuron.

[176]  K. Harris,et al.  Plasticity of perisynaptic astroglia during synaptogenesis in the mature rat hippocampus , 2007, Glia.

[177]  R. Wurtz,et al.  Brain circuits for the internal monitoring of movements. , 2008, Annual review of neuroscience.

[178]  Steven W. Flavell,et al.  Signaling mechanisms linking neuronal activity to gene expression and plasticity of the nervous system. , 2008, Annual review of neuroscience.