Synaptic stability and plasticity in a floating world

A fundamental feature of membranes is the lateral diffusion of lipids and proteins. Control of lateral diffusion provides a mechanism for regulating the structure and function of synapses. Single-particle tracking (SPT) has emerged as a powerful way to directly visualize these movements. SPT can reveal complex diffusive behaviors, which can be regulated by neuronal activity over time and space. Such is the case for neurotransmitter receptors, which are transiently stabilized at synapses by scaffolding molecules. This regulation provides new insight into mechanisms by which the dynamic equilibrium of receptor-scaffold assembly can be regulated. We will briefly review here recent data on this mechanism, which ultimately tunes the number of receptors at synapses and therefore synaptic strength.

[1]  G. Lynch,et al.  Integrins Modulate Fast Excitatory Transmission at Hippocampal Synapses* , 2003, The Journal of Biological Chemistry.

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

[3]  L. Kaczmarek,et al.  Matrix Metalloproteinase-9 Controls NMDA Receptor Surface Diffusion through Integrin β1 Signaling , 2009, The Journal of Neuroscience.

[4]  D. Choquet,et al.  NMDA receptor surface mobility depends on NR2A-2B subunits , 2006, Proceedings of the National Academy of Sciences.

[5]  M. Ehlers,et al.  Spine Microdomains for Postsynaptic Signaling and Plasticity , 2022 .

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

[7]  Paul C Bressloff,et al.  A dynamic corral model of receptor trafficking at a synapse. , 2009, Biophysical journal.

[8]  C. Specht,et al.  Gephyrin Oligomerization Controls GlyR Mobility and Synaptic Clustering , 2009, The Journal of Neuroscience.

[9]  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.

[10]  Lu Chen,et al.  Postsynaptic assembly induced by neurexin-neuroligin interaction and neurotransmitter , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Daniel Choquet,et al.  New Concepts in Synaptic Biology Derived from Single-Molecule Imaging , 2008, Neuron.

[12]  Akihiro Kusumi,et al.  Rapid hop diffusion of a G-protein-coupled receptor in the plasma membrane as revealed by single-molecule techniques. , 2005, Biophysical journal.

[13]  K. Mikoshiba,et al.  Activity-Dependent Tuning of Inhibitory Neurotransmission Based on GABAAR Diffusion Dynamics , 2009, Neuron.

[14]  D. Choquet,et al.  Multiple Routes for Glutamate Receptor Trafficking: Surface Diffusion and Membrane Traffic Cooperate to Bring Receptors to Synapses , 2006, Science's STKE.

[15]  A. Triller,et al.  Compatibility between itinerant synaptic receptors and stable postsynaptic structure. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[16]  M. Rasband,et al.  AnkyrinG is required for maintenance of the axon initial segment and neuronal polarity , 2008, The Journal of cell biology.

[17]  Daniel Choquet,et al.  Endocytic Trafficking and Recycling Maintain a Pool of Mobile Surface AMPA Receptors Required for Synaptic Potentiation , 2009, Neuron.

[18]  Daniel Choquet,et al.  Weak effect of membrane diffusion on the rate of receptor accumulation at adhesive contacts. , 2005, Biophysical journal.

[19]  H. Schindelin,et al.  Complex Formation between the Postsynaptic Scaffolding Protein Gephyrin, Profilin, and Mena: A Possible Link to the Microfilament System , 2003, The Journal of Neuroscience.

[20]  Berton A. Earnshaw,et al.  Diffusion-trapping model of receptor trafficking in dendrites. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[21]  M. Dahan,et al.  Cytoskeleton Regulation of Glycine Receptor Number at Synapses and Diffusion in the Plasma Membrane , 2006, The Journal of Neuroscience.

[22]  A. Triller,et al.  Activity-Dependent Movements of Postsynaptic Scaffolds at Inhibitory Synapses , 2006, The Journal of Neuroscience.

[23]  Ji Yu,et al.  Investigating Sub-Spine Actin Dynamics in Rat Hippocampal Neurons with Super-Resolution Optical Imaging , 2009, PloS one.

[24]  Daniel Choquet,et al.  Control of the Postsynaptic Membrane Viscosity , 2009, The Journal of Neuroscience.

[25]  Akihiro Kusumi,et al.  Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules. , 2005, Annual review of biophysics and biomolecular structure.

[26]  D. Chetkovich,et al.  Regulation of stargazin synaptic trafficking by C‐terminal PDZ ligand phosphorylation in bidirectional synaptic plasticity , 2010, Journal of neurochemistry.

[27]  A. Triller,et al.  Fast and reversible trapping of surface glycine receptors by gephyrin , 2001, Nature Neuroscience.

[28]  Pico Caroni,et al.  Dendritic spine morphology determines membrane-associated protein exchange between dendritic shafts and spine heads. , 2009, Cerebral cortex.

[29]  M. Pangalos,et al.  Synaptic GABAA receptors are directly recruited from their extrasynaptic counterparts , 2006, The EMBO journal.

[30]  A. Craig,et al.  Synapse-Specific Regulation of AMPA Receptor Subunit Composition by Activity , 2005, The Journal of Neuroscience.

[31]  Antoine Triller,et al.  Single‐particle tracking methods for the study of membrane receptors dynamics , 2009, The European journal of neuroscience.

[32]  C. Yap,et al.  Compartmentalizing the neuronal plasma membrane from axon initial segments to synapses. , 2009, International review of cell and molecular biology.

[33]  M. Dahan,et al.  Imaging the lateral diffusion of membrane molecules with quantum dots , 2007, Nature Protocols.

[34]  Paul C. Bressloff,et al.  Modeling the role of lateral membrane diffusion in AMPA receptor trafficking along a spiny dendrite , 2008, Journal of Computational Neuroscience.

[35]  Daniel Choquet,et al.  The excitatory postsynaptic density is a size exclusion diffusion environment , 2009, Neuropharmacology.

[36]  Daniel Choquet,et al.  Direct imaging of lateral movements of AMPA receptors inside synapses , 2003, The EMBO journal.

[37]  O. Pascual,et al.  Homeostatic Regulation of Synaptic GlyR Numbers Driven by Lateral Diffusion , 2008, Neuron.

[38]  D. Choquet,et al.  Regulation of AMPA receptor lateral movements , 2002, Nature.

[39]  O. Thoumine,et al.  Activity-independent and subunit-specific recruitment of functional AMPA receptors at neurexin/neuroligin contacts , 2008, Proceedings of the National Academy of Sciences.

[40]  Daniel Choquet,et al.  The Interaction between Stargazin and PSD-95 Regulates AMPA Receptor Surface Trafficking , 2007, Neuron.

[41]  J. Kauer,et al.  LTP of GABAergic synapses in the ventral tegmental area and beyond , 2008, The Journal of physiology.

[42]  M. Ehlers,et al.  Diffusional Trapping of GluR1 AMPA Receptors by Input-Specific Synaptic Activity , 2007, Neuron.

[43]  R. Iino,et al.  Accumulation of anchored proteins forms membrane diffusion barriers during neuronal polarization , 2003, Nature Cell Biology.

[44]  Maxime Dahan,et al.  Multiple association states between glycine receptors and gephyrin identified by SPT analysis. , 2007, Biophysical journal.

[45]  David Holcman,et al.  Modeling synaptic dynamics driven by receptor lateral diffusion. , 2006, Biophysical journal.

[46]  K. Thorn,et al.  Real-Time Imaging of Discrete Exocytic Events Mediating Surface Delivery of AMPA Receptors , 2007, The Journal of Neuroscience.

[47]  Philippe Rostaing,et al.  Diffusion Dynamics of Glycine Receptors Revealed by Single-Quantum Dot Tracking , 2003, Science.

[48]  C. Yap,et al.  Compartmentalizing the neuronal plasma membrane from axon initial segments to synapses. , 2009, International review of cell and molecular biology.

[49]  Daniel Choquet,et al.  Differential activity-dependent regulation of the lateral mobilities of AMPA and NMDA receptors , 2004, Nature Neuroscience.

[50]  Daniel Choquet,et al.  Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity , 2009, Nature Neuroscience.

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

[52]  A. Triller,et al.  Cellular Transport and Membrane Dynamics of the Glycine Receptor , 2009, Front. Mol. Neurosci..

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

[54]  C. Specht,et al.  Molecular dynamics of postsynaptic receptors and scaffold proteins , 2008, Current Opinion in Neurobiology.

[55]  Daniel Choquet,et al.  Active surface transport of metabotropic glutamate receptors through binding to microtubules and actin flow , 2003, Journal of Cell Science.

[56]  Daniel Choquet,et al.  NMDA Receptor Surface Trafficking and Synaptic Subunit Composition Are Developmentally Regulated by the Extracellular Matrix Protein Reelin , 2007, The Journal of Neuroscience.

[57]  A. Triller,et al.  Diffusion trajectory of an asymmetric object: information overlooked by the mean square displacement. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[58]  M. Rasband,et al.  Spectrin and Ankyrin-Based Cytoskeletons at Polarized Domains in Myelinated Axons , 2008, Experimental biology and medicine.

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

[60]  E. Gundelfinger,et al.  The Actin-Binding Protein Abp1 Controls Dendritic Spine Morphology and Is Important for Spine Head and Synapse Formation , 2008, The Journal of Neuroscience.

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