Heterosynaptic cross-talk of pre- and postsynaptic strengths along segments of dendrites

Dendrites are crucial for integrating incoming synaptic information. Individual dendritic branches are thought to constitute a signal processing unit, yet how neighbouring synapses shape the boundaries of functional dendritic units are not well understood. Here we addressed the cellular basis underlying the organization of the strengths of neighbouring Schaffer collateral-CA1 synapses by optical quantal analysis and spine size measurements. Inducing potentiation at clusters of spines produced NMDA receptor-dependent heterosynaptic plasticity. The direction of postsynaptic strength change showed distance-dependency to the stimulated synapses where proximal synapses predominantly depressed whereas distal synapses potentiated; potentiation and depression were regulated by CaMKII and calcineurin, respectively. By contrast, heterosynaptic presynaptic plasticity was confined to weakening of presynaptic strength of nearby synapses, which required CaMKII and the retrograde messenger nitric oxide. Our findings highlight the parallel engagement of multiple signalling pathways, each with characteristic spatial dynamics in shaping the local pattern of synaptic strengths.

[1]  C. Wierenga,et al.  Single Synapse LTP: A Matter of Context? , 2019, Front. Cell. Neurosci..

[2]  Y. Goda,et al.  Differential role of pre- and postsynaptic neurons in the activity-dependent control of synaptic strengths across dendrites , 2019, PLoS biology.

[3]  N. Emptage,et al.  Optical Quantal Analysis Using Ca2+ Indicators: A Robust Method for Assessing Transmitter Release Probability at Excitatory Synapses by Imaging Single Glutamate Release Events , 2019, Front. Synaptic Neurosci..

[4]  D. Fitzpatrick,et al.  Functional Synaptic Architecture of Callosal Inputs in Mouse Primary Visual Cortex , 2019, Neuron.

[5]  M. Sur,et al.  Locally coordinated synaptic plasticity of visual cortex neurons in vivo , 2018, Science.

[6]  Josh L. Morgan,et al.  A Fine-Scale Functional Logic to Convergence from Retina to Thalamus , 2018, Cell.

[7]  David Fitzpatrick,et al.  Local Order within Global Disorder: Synaptic Architecture of Visual Space , 2017, Neuron.

[8]  N. Emptage,et al.  Glutamate is required for depression but not potentiation of long-term presynaptic function , 2017, eLife.

[9]  T. Vogels,et al.  Synaptic Transmission Optimization Predicts Expression Loci of Long-Term Plasticity , 2017, Neuron.

[10]  J. McNamara,et al.  Rho GTPase complementation underlies BDNF-dependent homo- and heterosynaptic plasticity , 2016, Nature.

[11]  Thomas A. Blanpied,et al.  A transsynaptic nanocolumn aligns neurotransmitter release to receptors , 2016, Nature.

[12]  Z. Qiu,et al.  Coordinated Spine Pruning and Maturation Mediated by Inter-Spine Competition for Cadherin/Catenin Complexes , 2015, Cell.

[13]  Forrest Collman,et al.  Knowing a synapse when you see one , 2015, Front. Neuroanat..

[14]  Christian Lohmann,et al.  Spontaneous Activity Drives Local Synaptic Plasticity In Vivo , 2015, Neuron.

[15]  Ryohei Yasuda,et al.  Biochemical Computation for Spine Structural Plasticity , 2015, Neuron.

[16]  L. Parajuli,et al.  Heterosynaptic structural plasticity on local dendritic segments of hippocampal CA1 neurons. , 2015, Cell reports.

[17]  Tobias Bonhoeffer,et al.  Balance and Stability of Synaptic Structures during Synaptic Plasticity , 2014, Neuron.

[18]  G. Buzsáki,et al.  The log-dynamic brain: how skewed distributions affect network operations , 2014, Nature Reviews Neuroscience.

[19]  J. Magee,et al.  Structured Synaptic Connectivity between Hippocampal Regions , 2014, Neuron.

[20]  J. Simon Wiegert,et al.  Long-term depression triggers the selective elimination of weakly integrated synapses , 2013, Proceedings of the National Academy of Sciences.

[21]  Dominique Muller,et al.  Nitric oxide mediates local activity-dependent excitatory synapse development , 2013, Proceedings of the National Academy of Sciences.

[22]  K. Fox,et al.  The role of nitric oxide in pre-synaptic plasticity and homeostasis , 2013, Front. Cell. Neurosci..

[23]  Jun Noguchi,et al.  GABA promotes the competitive selection of dendritic spines by controlling local Ca2+ signaling , 2013, Nature Neuroscience.

[24]  W. Greenough,et al.  Motor Skill Training Induces Coordinated Strengthening and Weakening between Neighboring Synapses , 2013, The Journal of Neuroscience.

[25]  Masanobu Kano,et al.  Nonlinear decoding and asymmetric representation of neuronal input information by CaMKIIα and calcineurin. , 2013, Cell reports.

[26]  M. Baudry,et al.  Simultaneous Monitoring of Presynaptic Transmitter Release and Postsynaptic Receptor Trafficking Reveals an Enhancement of Presynaptic Activity in Metabotropic Glutamate Receptor-Mediated Long-Term Depression , 2013, The Journal of Neuroscience.

[27]  D. Attwell,et al.  Synaptic Energy Use and Supply , 2012, Neuron.

[28]  Kevin W Eliceiri,et al.  NIH Image to ImageJ: 25 years of image analysis , 2012, Nature Methods.

[29]  A. Cardona,et al.  Fiji: an open-source platform for biological-image analysis , 2012, Nature Methods.

[30]  Kristina D. Micheva,et al.  Deep molecular diversity of mammalian synapses: why it matters and how to measure it , 2012, Nature Reviews Neuroscience.

[31]  Christian Lohmann,et al.  Synaptic clustering during development and learning: the why, when, and how , 2012, Front. Mol. Neurosci..

[32]  Lu Chen Faculty Opinions recommendation of Repetitive motor learning induces coordinated formation of clustered dendritic spines in vivo. , 2012 .

[33]  T. Branco,et al.  Recruitment of resting vesicles into recycling pools supports NMDA receptor-dependent synaptic potentiation in cultured hippocampal neurons , 2012, The Journal of physiology.

[34]  Norio Matsuki,et al.  Locally Synchronized Synaptic Inputs , 2012, Science.

[35]  Tobias Bonhoeffer,et al.  Activity-Dependent Clustering of Functional Synaptic Inputs on Developing Hippocampal Dendrites , 2011, Neuron.

[36]  Nathalie L Rochefort,et al.  Functional mapping of single spines in cortical neurons in vivo , 2011, Nature.

[37]  L. Humphreys,et al.  Neuronal activity drives matching of pre- and postsynaptic function during synapse maturation , 2011, Nature Neuroscience.

[38]  Kristen M Harris,et al.  Coordination of size and number of excitatory and inhibitory synapses results in a balanced structural plasticity along mature hippocampal CA1 dendrites during LTP , 2011, Hippocampus.

[39]  P. Caroni,et al.  Temporally matched subpopulations of selectively interconnected principal neurons in the hippocampus , 2011, Nature Neuroscience.

[40]  Susumu Tonegawa,et al.  The Dendritic Branch Is the Preferred Integrative Unit for Protein Synthesis-Dependent LTP , 2011, Neuron.

[41]  M. Häusser,et al.  The single dendritic branch as a fundamental functional unit in the nervous system , 2010, Current Opinion in Neurobiology.

[42]  Hongbo Jia,et al.  Dendritic organization of sensory input to cortical neurons in vivo , 2010, Nature.

[43]  M. J. Friedlander,et al.  Plasticity between Neuronal Pairs in Layer 4 of Visual Cortex Varies with Synapse State , 2009, The Journal of Neuroscience.

[44]  Y. Goda,et al.  Activity-dependent coordination of presynaptic release probability and postsynaptic GluR2 abundance at single synapses , 2008, Proceedings of the National Academy of Sciences.

[45]  T. Branco,et al.  Local Dendritic Activity Sets Release Probability at Hippocampal Synapses , 2008, Neuron.

[46]  Karel Svoboda,et al.  The Spread of Ras Activity Triggered by Activation of a Single Dendritic Spine , 2008, Science.

[47]  A. Rodríguez-Contreras,et al.  Learning Drives Differential Clustering of Axodendritic Contacts in the Barn Owl Auditory System , 2008, The Journal of Neuroscience.

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

[49]  J. Nadal,et al.  What can we learn from synaptic weight distributions? , 2007, Trends in Neurosciences.

[50]  Robert J Richardson,et al.  Slow Presynaptic and Fast Postsynaptic Components of Compound Long-Term Potentiation , 2007, The Journal of Neuroscience.

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

[52]  S. Tonegawa,et al.  A clustered plasticity model of long-term memory engrams , 2006, Nature Reviews Neuroscience.

[53]  E. Schuman,et al.  Miniature Neurotransmission Stabilizes Synaptic Function via Tonic Suppression of Local Dendritic Protein Synthesis , 2006, Cell.

[54]  P. Stanton,et al.  Imaging LTP of presynaptic release of FM1‐43 from the rapidly recycling vesicle pool of Schaffer collateral–CA1 synapses in rat hippocampal slices , 2005, The European journal of neuroscience.

[55]  R. Morris,et al.  Competing for Memory Hippocampal LTP under Regimes of Reduced Protein Synthesis , 2004, Neuron.

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

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

[58]  P. Stanton,et al.  Long-Term Depression of Presynaptic Release from the Readily Releasable Vesicle Pool Induced by NMDA Receptor-Dependent Retrograde Nitric Oxide , 2003, The Journal of Neuroscience.

[59]  S. Royer,et al.  Conservation of total synaptic weight through balanced synaptic depression and potentiation , 2003, Nature.

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

[61]  Bartlett W. Mel,et al.  Pyramidal Neuron as Two-Layer Neural Network , 2003, Neuron.

[62]  Yasushi Miyashita,et al.  Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons , 2001, Nature Neuroscience.

[63]  Bartlett W. Mel,et al.  Impact of Active Dendrites and Structural Plasticity on the Memory Capacity of Neural Tissue , 2001, Neuron.

[64]  P. Stanton,et al.  Induction of hippocampal LTD requires nitric-oxide-stimulated PKG activity and Ca2+ release from cyclic ADP-ribose-sensitive stores. , 1999, Journal of neurophysiology.

[65]  W. Singer,et al.  Relations Between Long‐term Synaptic Modifications and Paired‐pulse Interactions in the Rat Neocortex , 1997, The European journal of neuroscience.

[66]  F. Engert,et al.  Synapse specificity of long-term potentiation breaks down at short distances , 1997, Nature.

[67]  E. Kandel,et al.  Nitric Oxide Acts Directly in the Presynaptic Neuron to Produce Long-Term Potentiationin Cultured Hippocampal Neurons , 1996, Cell.

[68]  P. Stanton,et al.  Distinct synaptic loci of Ca2+/calmodulin-dependent protein kinase II necessary for long-term potentiation and depression. , 1996, Journal of neurophysiology.

[69]  Massimo Scanziani,et al.  Role of intercellular interactions in heterosynaptic long-term depression , 1996, Nature.

[70]  E. Kandel,et al.  Nitric oxide and cGMP can produce either synaptic depression or potentiation depending on the frequency of presynaptic stimulation in the hippocampus. , 1994, Neuroreport.

[71]  D. Madison,et al.  Locally distributed synaptic potentiation in the hippocampus. , 1994, Science.

[72]  T. Bliss,et al.  A synaptic model of memory: long-term potentiation in the hippocampus , 1993, Nature.

[73]  Bartlett W. Mel The Clusteron: Toward a Simple Abstraction for a Complex Neuron , 1991, NIPS.

[74]  G. Lynch,et al.  Heterosynaptic depression: a postsynaptic correlate of long-term potentiation , 1977, Nature.

[75]  P. Stanton,et al.  Nitric‐oxide‐guanylyl‐cyclase‐dependent and ‐independent components of multiple forms of long‐term synaptic depression , 1997, Hippocampus.