Structural dynamics of dendritic spines in memory and cognition

Recent studies show that dendritic spines are dynamic structures. Their rapid creation, destruction and shape-changing are essential for short- and long-term plasticity at excitatory synapses on pyramidal neurons in the cerebral cortex. The onset of long-term potentiation, spine-volume growth and an increase in receptor trafficking are coincident, enabling a 'functional readout' of spine structure that links the age, size, strength and lifetime of a synapse. Spine dynamics are also implicated in long-term memory and cognition: intrinsic fluctuations in volume can explain synapse maintenance over long periods, and rapid, activity-triggered plasticity can relate directly to cognitive processes. Thus, spine dynamics are cellular phenomena with important implications for cognition and memory. Furthermore, impaired spine dynamics can cause psychiatric and neurodevelopmental disorders.

[1]  M. Frerking,et al.  Spine Expansion and Stabilization Associated with Long-Term Potentiation , 2008, The Journal of Neuroscience.

[2]  G. Shepherd,et al.  Transient and Persistent Dendritic Spines in the Neocortex In Vivo , 2005, Neuron.

[3]  Karel Svoboda,et al.  Rapid Redistribution of Synaptic PSD-95 in the Neocortex In Vivo , 2006, PLoS biology.

[4]  Lamme Vaf,et al.  Why visual attention and awareness are different , 2003 .

[5]  Susumu Tonegawa,et al.  Altered Cortical Synaptic Morphology and Impaired Memory Consolidation in Forebrain- Specific Dominant-Negative PAK Transgenic Mice , 2004, Neuron.

[6]  H. Kasai,et al.  Generation, elimination and weight fluctuations of synapses in the cerebral cortex , 2009 .

[7]  M. Sheng,et al.  Quaternary Structure, Protein Dynamics, and Synaptic Function of SAP97 Controlled by L27 Domain Interactions , 2004, Neuron.

[8]  Peter Somogyi,et al.  Cell Type and Pathway Dependence of Synaptic AMPA Receptor Number and Variability in the Hippocampus , 1998, Neuron.

[9]  A M McIntosh,et al.  Connecting the brain and new drug targets for schizophrenia. , 2009, Current pharmaceutical design.

[10]  R. Yuste,et al.  Developmental regulation of spine motility in the mammalian central nervous system. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[11]  John Lisman,et al.  Synaptic Strength of Individual Spines Correlates with Bound Ca2+–Calmodulin-Dependent Kinase II , 2007, The Journal of Neuroscience.

[12]  C. Gray.  The Temporal Correlation Hypothesis of Visual Feature Integration Still Alive and Well , 1999, Neuron.

[13]  Robert Plomin,et al.  Intelligence: genetics, genes, and genomics. , 2004, Journal of personality and social psychology.

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

[15]  Jun Noguchi,et al.  Spine-Neck Geometry Determines NMDA Receptor-Dependent Ca2+ Signaling in Dendrites , 2005, Neuron.

[16]  Henry C. Tuckwell,et al.  Introduction to theoretical neurobiology , 1988 .

[17]  Karel Svoboda,et al.  Experience-dependent and cell-type-specific spine growth in the neocortex , 2006, Nature.

[18]  Bartlett W. Mel,et al.  Cortical rewiring and information storage , 2004, Nature.

[19]  J. Wixted,et al.  Genuine power curves in forgetting: A quantitative analysis of individual subject forgetting functions , 1997, Memory & cognition.

[20]  K. Svoboda,et al.  Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex , 2002, Nature.

[21]  Kaoru Inokuchi,et al.  Input-Specific Spine Entry of Soma-Derived Vesl-1S Protein Conforms to Synaptic Tagging , 2009, Science.

[22]  K. Sobue,et al.  Rapid Redistribution of the Postsynaptic Density Protein PSD-Zip45 (Homer 1c) and Its Differential Regulation by NMDA Receptors and Calcium Channels , 2001, The Journal of Neuroscience.

[23]  Takeharu Nagai,et al.  Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity , 2004, Nature Neuroscience.

[24]  T. Südhof.  Neuroligins and neurexins link synaptic function to cognitive disease , 2008, Nature.

[25]  Kazuyuki Aihara,et al.  Discharge Synchrony during the Transition of Behavioral Goal Representations Encoded by Discharge Rates of Prefrontal Neurons , 2008, Cerebral cortex.

[26]  D. Hubel,et al.  Receptive fields of single neurones in the cat's striate cortex , 1959, The Journal of physiology.

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

[28]  Roberto Malinow,et al.  AMPA Receptor Incorporation into Synapses during LTP: The Role of Lateral Movement and Exocytosis , 2009, Neuron.

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

[30]  W. Gan,et al.  Stably maintained dendritic spines are associated with lifelong memories , 2009, Nature.

[31]  P. Kloeden,et al.  Numerical Solution of Stochastic Differential Equations , 1992 .

[32]  Jun Noguchi,et al.  The Subspine Organization of Actin Fibers Regulates the Structure and Plasticity of Dendritic Spines , 2008, Neuron.

[33]  H. Kasai,et al.  Vacuolar sequential exocytosis of large dense‐core vesicles in adrenal medulla , 2006, The EMBO journal.

[34]  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.

[35]  S. Kaech,et al.  Volatile anesthetics block actin-based motility in dendritic spines. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[36]  C. von der Malsburg.  The what and why of binding: the modeler's perspective. , 1999, Neuron.

[37]  M. Colonnese,et al.  Developmental period for N‐methyl‐D‐aspartate (NMDA) receptor‐dependent synapse elimination correlated with visuotopic map refinement , 2006, The Journal of comparative neurology.

[38]  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.

[39]  D. Choquet,et al.  [Surface mobility of postsynaptic AMPARs tunes synaptic transmission]. , 2008, Medecine sciences : M/S.

[40]  Paul J. Harrison.  The neuropathology of schizophrenia , 2008 .

[41]  Thomas G. Oertner,et al.  Differential distribution of endoplasmic reticulum controls metabotropic signaling and plasticity at hippocampal synapses , 2009, Proceedings of the National Academy of Sciences.

[42]  R. Weinberg,et al.  Immunogold localization of AMPA and NMDA receptors in somatic sensory cortex of albino rat , 1999, The Journal of comparative neurology.

[43]  Karel Svoboda,et al.  NMDA Receptor Subunit-Dependent [Ca2+] Signaling in Individual Hippocampal Dendritic Spines , 2005, The Journal of Neuroscience.

[44]  Karel Svoboda,et al.  Abnormal Development of Dendritic Spines inFMR1 Knock-Out Mice , 2001, The Journal of Neuroscience.

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

[46]  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.

[47]  B. Libet.  Mind Time: The Temporal Factor in Consciousness , 2004 .

[48]  N. N. Kasri,et al.  Rho-linked genes and neurological disorders , 2008, Pflügers Archiv - European Journal of Physiology.

[49]  Susumu Tonegawa,et al.  Translational Regulatory Mechanisms in Persistent Forms of Synaptic Plasticity , 2004, Neuron.

[50]  N. Block,et al.  How can we find the neural correlate of consciousness? , 1996, Trends in neurosciences.

[51]  Dominique Muller,et al.  LTP Promotes a Selective Long-Term Stabilization and Clustering of Dendritic Spines , 2008, PLoS biology.

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

[53]  Mark F Bear,et al.  Smaller Dendritic Spines, Weaker Synaptic Transmission, but Enhanced Spatial Learning in Mice Lacking Shank1 , 2008, The Journal of Neuroscience.

[54]  J. Searle.  Mind: A Brief Introduction , 2004 .

[55]  H. Risken.  Fokker-Planck Equation , 1984 .

[56]  H. Kasai,et al.  Structure–stability–function relationships of dendritic spines , 2003, Trends in Neurosciences.

[57]  K. Svoboda,et al.  Experience-dependent structural synaptic plasticity in the mammalian brain , 2009, Nature Reviews Neuroscience.

[58]  S. Cajal,et al.  Histology of the Nervous System , 1911 .

[59]  Seok-Jin R. Lee,et al.  Activation of CaMKII in single dendritic spines during long-term potentiation , 2009, Nature.

[60]  D. O. Hebb,et al.  The organization of behavior , 1988 .

[61]  Kristen M Harris,et al.  Dendritic Spine Pathology: Cause or Consequence of Neurological Disorders? , 2002, Brain Research Reviews.

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

[63]  S. Dudek,et al.  Synapse elimination accompanies functional plasticity in hippocampal neurons , 2008, Proceedings of the National Academy of Sciences.

[64]  D. Bredt,et al.  AMPA Receptor Subunit-Specific Regulation by a Distinct Family of Type II TARPs , 2008, Neuron.

[65]  C. Koch,et al.  Consciousness and neuroscience. , 1998, Cerebral cortex.

[66]  H. Wigström,et al.  Long-term potentiation in the hippocampal CA1 region: its induction and early temporal development. , 1990, Progress in brain research.

[67]  D. Lewis,et al.  Neuroplasticity of Neocortical Circuits in Schizophrenia , 2008, Neuropsychopharmacology.

[68]  M. Egan,et al.  Schizophrenia, just the facts What do we know, how well do we know it? , 1988, Schizophrenia Research.

[69]  H. Ebbinghaus.  Uber das Gedachtnis , 1996 .

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

[71]  Karel Svoboda,et al.  Locally dynamic synaptic learning rules in pyramidal neuron dendrites , 2007, Nature.

[72]  J. Kao,et al.  Long-term potentiation of exogenous glutamate responses at single dendritic spines. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[73]  Larry J Seidman,et al.  Premorbid IQ in schizophrenia: a meta-analytic review. , 2008, The American journal of psychiatry.

[74]  Bita Moghaddam,et al.  Bringing Order to the Glutamate Chaos in Schizophrenia , 2003, Neuron.

[75]  C. H. Bailey,et al.  The anatomy of a memory: convergence of results across a diversity of tests , 1988, Trends in Neurosciences.

[76]  Yi Zuo,et al.  Long-term sensory deprivation prevents dendritic spine loss in primary somatosensory cortex , 2005, Nature.

[77]  D. Purpura,et al.  Dendritic Spine "Dysgenesis" and Mental Retardation , 1974, Science.

[78]  T. Bonhoeffer,et al.  Experience leaves a lasting structural trace in cortical circuits , 2008, Nature.

[79]  Raag D. Airan,et al.  Temporally precise in vivo control of intracellular signalling , 2009, Nature.

[80]  J. Coyle,et al.  The emerging role of glutamate in the pathophysiology and treatment of schizophrenia. , 2001, The American journal of psychiatry.

[81]  Christian Rosenmund,et al.  Definition of the Readily Releasable Pool of Vesicles at Hippocampal Synapses , 1996, Neuron.

[82]  Haruo Kasai,et al.  Protein Synthesis and Neurotrophin-Dependent Structural Plasticity of Single Dendritic Spines , 2008, Science.

[83]  R. Nicoll,et al.  Long-term potentiation--a decade of progress? , 1999, Science.

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

[85]  A. Sawa,et al.  Postsynaptic density: a key convergent site for schizophrenia susceptibility factors and possible target for drug development. , 2007, Drugs of today.

[86]  D H Perkel,et al.  The function of dendritic spines: a review of theoretical issues. , 1985, Behavioral and neural biology.

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

[88]  R. Roberts,et al.  Reduced striatal spine size in schizophrenia: a postmortem ultrastructural study , 1996, Neuroreport.

[89]  Leonard T. Troland.  The mystery of mind , 1926 .

[90]  R. Huganir,et al.  Synapse-specific regulation of AMPA receptor function by PSD-95 , 2006, Proceedings of the National Academy of Sciences.

[91]  H. Kasai,et al.  Principles of Long-Term Dynamics of Dendritic Spines , 2008, The Journal of Neuroscience.

[92]  R. Desimone,et al.  High-Frequency, Long-Range Coupling Between Prefrontal and Visual Cortex During Attention , 2009, Science.

[93]  Willie F. Tobin,et al.  Rapid formation and selective stabilization of synapses for enduring motor memories , 2009, Nature.

[94]  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.

[95]  R. Yuste,et al.  Cortical area and species differences in dendritic spine morphology , 2002, Journal of neurocytology.

[96]  Paul J. Harrison,et al.  Six degrees of separation: on the prior probability that schizophrenia susceptibility genes converge on synapses, glutamate and NMDA receptors , 2006, Molecular Psychiatry.

[97]  K. Svoboda,et al.  Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo , 2000, Nature.

[98]  M. Keshavan,et al.  Schizophrenia, “just the facts” 4. Clinical features and conceptualization , 2009, Schizophrenia Research.

[99]  C. Gilbert,et al.  Axons and Synaptic Boutons Are Highly Dynamic in Adult Visual Cortex , 2006, Neuron.

[100]  D. Muller,et al.  The Mental Retardation Protein PAK3 Contributes to Synapse Formation and Plasticity in Hippocampus , 2004, The Journal of Neuroscience.

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

[102]  F. Leiss,et al.  Characterization of dendritic spines in the Drosophila central nervous system , 2009, Developmental neurobiology.

[103]  Qiang Zhou,et al.  Independent Expression of Synaptic and Morphological Plasticity Associated with Long-Term Depression , 2007, The Journal of Neuroscience.

[104]  W. Abraham.  How long will long-term potentiation last? , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[106]  M. Keshavan,et al.  Schizophrenia, “just the facts”: What we know in 2008 Part 3: Neurobiology , 2008, Schizophrenia Research.

[107]  N. Kasthuri,et al.  Long-term dendritic spine stability in the adult cortex , 2002, Nature.

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

[109]  Aude Oliva,et al.  Detecting changes in real-world objects: The relationship between visual long-term memory and change blindness , 2009, Communicative & integrative biology.

[110]  J. Magee,et al.  Mechanism of the distance‐dependent scaling of Schaffer collateral synapses in rat CA1 pyramidal neurons , 2003, The Journal of physiology.

[111]  P. Penzes,et al.  Dendritic spine dynamics – a key role for kalirin-7 , 2008, Trends in Neurosciences.

[112]  Roberto Malinow,et al.  Synaptic AMPA Receptor Plasticity and Behavior , 2009, Neuron.

[113]  H. J. Gamble.  Trends in Neurosciences , 1980 .

[114]  M. Imbert,et al.  The primary visual cortex in the mouse: Receptive field properties and functional organization , 2004, Experimental Brain Research.

[115]  Ger J. A. Ramakers,et al.  Rho proteins, mental retardation and the cellular basis of cognition , 2002, Trends in Neurosciences.

[116]  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.

[117]  R. Hoffman,et al.  Schizophrenia as a disorder of developmentally reduced synaptic connectivity. , 2000, Archives of general psychiatry.

[118]  M. Ehlers,et al.  Spine microdomains for postsynaptic signaling and plasticity. , 2009, Trends in cell biology.

[119]  Karel Svoboda,et al.  Rapid Functional Maturation of Nascent Dendritic Spines , 2009, Neuron.

[120]  T. Pollard,et al.  Cellular Motility Driven by Assembly and Disassembly of Actin Filaments , 2003, Cell.