Homeostatic role of heterosynaptic plasticity: models and experiments

Homosynaptic Hebbian-type plasticity provides a cellular mechanism of learning and refinement of connectivity during development in a variety of biological systems. In this review we argue that a complimentary form of plasticity—heterosynaptic plasticity—represents a necessary cellular component for homeostatic regulation of synaptic weights and neuronal activity. The required properties of a homeostatic mechanism which acutely constrains the runaway dynamics imposed by Hebbian associative plasticity have been well-articulated by theoretical and modeling studies. Such mechanism(s) should robustly support the stability of operation of neuronal networks and synaptic competition, include changes at non-active synapses, and operate on a similar time scale to Hebbian-type plasticity. The experimentally observed properties of heterosynaptic plasticity have introduced it as a strong candidate to fulfill this homeostatic role. Subsequent modeling studies which incorporate heterosynaptic plasticity into model neurons with Hebbian synapses (utilizing an STDP learning rule) have confirmed its ability to robustly provide stability and competition. In contrast, properties of homeostatic synaptic scaling, which is triggered by extreme and long lasting (hours and days) changes of neuronal activity, do not fit two crucial requirements for a hypothetical homeostatic mechanism needed to provide stability of operation in the face of on-going synaptic changes driven by Hebbian-type learning rules. Both the trigger and the time scale of homeostatic synaptic scaling are fundamentally different from those of the Hebbian-type plasticity. We conclude that heterosynaptic plasticity, which is triggered by the same episodes of strong postsynaptic activity and operates on the same time scale as Hebbian-type associative plasticity, is ideally suited to serve a homeostatic role during on-going synaptic plasticity.

[1]  Steve M. Potter,et al.  Upward synaptic scaling is dependent on neurotransmission rather than spiking , 2015, Nature Communications.

[2]  M. Volgushev,et al.  Adenosine effects on inhibitory synaptic transmission and excitation–inhibition balance in the rat neocortex , 2015, The Journal of physiology.

[3]  Maxim Bazhenov,et al.  The Impact of Cortical Deafferentation on the Neocortical Slow Oscillation , 2014, The Journal of Neuroscience.

[4]  M. Volgushev,et al.  Heterosynaptic Plasticity , 2014, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[5]  M. Bazhenov,et al.  A Spiking Network Model of Decision Making Employing Rewarded STDP , 2014, PloS one.

[6]  M. Volgushev,et al.  Modulation of synaptic transmission by adenosine in layer 2/3 of the rat visual cortex in vitro , 2014, Neuroscience.

[7]  D. Becker,et al.  Tumor necrosis factor alpha maintains denervation-induced homeostatic synaptic plasticity of mouse dentate granule cells , 2013, Front. Cell. Neurosci..

[8]  Wulfram Gerstner,et al.  Synaptic Plasticity in Neural Networks Needs Homeostasis with a Fast Rate Detector , 2013, PLoS Comput. Biol..

[9]  M. Diesmann,et al.  NMDA-receptor inhibition increases spine stability of denervated mouse dentate granule cells and accelerates spine density recovery following entorhinal denervation in vitro , 2013, Neurobiology of Disease.

[10]  G. Davis Homeostatic Signaling and the Stabilization of Neural Function , 2013, Neuron.

[11]  Georg B. Keller,et al.  Synaptic Scaling and Homeostatic Plasticity in the Mouse Visual Cortex In Vivo , 2013, Neuron.

[12]  Christopher M. Lee,et al.  Heterosynaptic Plasticity Prevents Runaway Synaptic Dynamics , 2013, The Journal of Neuroscience.

[13]  J. Moyer,et al.  Learning to learn – Intrinsic plasticity as a metaplasticity mechanism for memory formation , 2013, Neurobiology of Learning and Memory.

[14]  D. Feldman,et al.  Spike Timing-Dependent Plasticity , 2013 .

[15]  Mark C. W. van Rossum,et al.  Probabilistic inference of short-term synaptic plasticity in neocortical microcircuits , 2013, Front. Comput. Neurosci..

[16]  G. Turrigiano,et al.  Synaptic and Intrinsic Homeostatic Mechanisms Cooperate to Increase L2/3 Pyramidal Neuron Excitability during a Late Phase of Critical Period Plasticity , 2013, The Journal of Neuroscience.

[17]  Yuchio Yanagawa,et al.  Reciprocal Homosynaptic and Heterosynaptic Long-Term Plasticity of Corticogeniculate Projection Neurons in Layer VI of the Mouse Visual Cortex , 2013, The Journal of Neuroscience.

[18]  Mark J. Wall,et al.  Adenosine A1 receptor activation mediates the developmental shift at layer 5 pyramidal cell synapses and is a determinant of mature synaptic strength , 2013, The Journal of physiology.

[19]  Lu Chen,et al.  Chronic Inactivation of a Neural Circuit Enhances LTP by Inducing Silent Synapse Formation , 2013, The Journal of Neuroscience.

[20]  Y. Goda,et al.  Homeostatic synaptic plasticity: from single synapses to neural circuits , 2012, Current Opinion in Neurobiology.

[21]  Christopher M. Lee,et al.  Heterosynaptic plasticity induced by intracellular tetanization in layer 2/3 pyramidal neurons in rat auditory cortex , 2012, The Journal of physiology.

[22]  Wei Liu,et al.  Neuronal Adenosine Release, and Not Astrocytic Atp Release, Mediates Feedback Inhibition of Excitatory Activity. Adenosine Release during Seizures Attenuates Gabaa Receptor-mediated Depolarization. Adenosine and Seizure Termination: Endogenous Mechanisms , 2022 .

[23]  Yotam Luz,et al.  Balancing Feed-Forward Excitation and Inhibition via Hebbian Inhibitory Synaptic Plasticity , 2012, PLoS Comput. Biol..

[24]  Henning Sprekeler,et al.  Inhibitory Plasticity Balances Excitation and Inhibition in Sensory Pathways and Memory Networks , 2011, Science.

[25]  Michael C. Crair,et al.  Visual Map Development Depends On The Temporal Pattern of Binocular Activity in Mice , 2011, Nature Neuroscience.

[26]  Matthieu Gilson,et al.  Stability versus Neuronal Specialization for STDP: Long-Tail Weight Distributions Solve the Dilemma , 2011, PloS one.

[27]  Maxim Bazhenov,et al.  Topological basis of epileptogenesis in a model of severe cortical trauma. , 2011, Journal of neurophysiology.

[28]  Maxim Bazhenov,et al.  Pattern of trauma determines the threshold for epileptic activity in a model of cortical deafferentation , 2011, Proceedings of the National Academy of Sciences.

[29]  G. Turrigiano Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement. , 2011, Annual review of neuroscience.

[30]  Baktash Babadi,et al.  Intrinsic Stability of Temporally Shifted Spike-Timing Dependent Plasticity , 2010, PLoS Comput. Biol..

[31]  Mu Zhou,et al.  Fine-tuning of pre-balanced excitation and inhibition during auditory cortical development , 2010, Nature.

[32]  Christoph E. Schreiner,et al.  Developmental sensory experience balances cortical excitation and inhibition , 2010, Nature.

[33]  Niraj S. Desai,et al.  Homeostatic Plasticity and STDP: Keeping a Neuron's Cool in a Fluctuating World , 2010, Front. Syn. Neurosci..

[34]  A. E. Fink,et al.  Short Trains of Theta Frequency Stimulation Enhance CA1 Pyramidal Neuron Excitability in the Absence of Synaptic Potentiation , 2009, The Journal of Neuroscience.

[35]  D. Feldman Synaptic mechanisms for plasticity in neocortex. , 2009, Annual review of neuroscience.

[36]  M. Volgushev,et al.  Heterosynaptic plasticity in the neocortex , 2009, Experimental Brain Research.

[37]  Evan S. Schaffer,et al.  Inhibitory Stabilization of the Cortical Network Underlies Visual Surround Suppression , 2009, Neuron.

[38]  Michael M. Halassa,et al.  Astrocytic Modulation of Sleep Homeostasis and Cognitive Consequences of Sleep Loss , 2009, Neuron.

[39]  Mark J. Wall,et al.  Activity-Dependent Release of Adenosine: A Critical Re-Evaluation of Mechanism , 2008, Current neuropharmacology.

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

[41]  T. Tsumoto,et al.  Roles of Endocannabinoids in Heterosynaptic Long-Term Depression of Excitatory Synaptic Transmission in Visual Cortex of Young Mice , 2008, The Journal of Neuroscience.

[42]  Michael Okun,et al.  Instantaneous correlation of excitation and inhibition during ongoing and sensory-evoked activities , 2008, Nature Neuroscience.

[43]  P. J. Sjöström,et al.  Dendritic excitability and synaptic plasticity. , 2008, Physiological reviews.

[44]  Terrence J. Sejnowski,et al.  Synaptic Learning Rules and Sparse Coding in a Model Sensory System , 2008, PLoS Comput. Biol..

[45]  G. Turrigiano,et al.  Rapid Synaptic Scaling Induced by Changes in Postsynaptic Firing , 2008, Neuron.

[46]  Maxim Bazhenov,et al.  Pathological Effect of Homeostatic Synaptic Scaling on Network Dynamics in Diseases of the Cortex , 2008, The Journal of Neuroscience.

[47]  Larissa A. Jarzylo,et al.  Homeostatic regulation of AMPA receptor expression at single hippocampal synapses , 2008, Proceedings of the National Academy of Sciences.

[48]  Alison L. Barth,et al.  Ongoing in Vivo Experience Triggers Synaptic Metaplasticity in the Neocortex , 2008, Science.

[49]  N. Spruston,et al.  Dendritic spikes induce single-burst long-term potentiation , 2007, Proceedings of the National Academy of Sciences.

[50]  Markus Diesmann,et al.  Spike-Timing-Dependent Plasticity in Balanced Random Networks , 2007, Neural Computation.

[51]  W. Maass,et al.  Self-tuning of neural circuits through short-term synaptic plasticity. , 2007, Journal of neurophysiology.

[52]  J. Kauer,et al.  Opioids block long-term potentiation of inhibitory synapses , 2007, Nature.

[53]  K. Fox,et al.  Presynaptic efficacy directs normalization of synaptic strength in layer 2/3 rat neocortex after paired activity. , 2007, Journal of neurophysiology.

[54]  M. Kano,et al.  Endocannabinoids and Synaptic Function in the CNS , 2007, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[55]  Peter Wenner,et al.  Sensing and expressing homeostatic synaptic plasticity , 2007, Trends in Neurosciences.

[56]  Uwe Heinemann,et al.  Low‐frequency stimulation of the direct cortical input to area CA1 induces homosynaptic LTD and heterosynaptic LTP in the rat hippocampal–entorhinal cortex slice preparation , 2007, The European journal of neuroscience.

[57]  H. Abarbanel,et al.  Spike-timing-dependent plasticity of inhibitory synapses in the entorhinal cortex. , 2006, Journal of neurophysiology.

[58]  B. Sakmann,et al.  Spine Ca2+ Signaling in Spike-Timing-Dependent Plasticity , 2006, The Journal of Neuroscience.

[59]  Johannes J. Letzkus,et al.  Learning Rules for Spike Timing-Dependent Plasticity Depend on Dendritic Synapse Location , 2006, The Journal of Neuroscience.

[60]  P. J. Sjöström,et al.  A Cooperative Switch Determines the Sign of Synaptic Plasticity in Distal Dendrites of Neocortical Pyramidal Neurons , 2006, Neuron.

[61]  Idan Segev,et al.  The interplay between homeostatic synaptic plasticity and functional dendritic compartments. , 2006, Journal of neurophysiology.

[62]  Yoko Yamaguchi,et al.  Conserving total synaptic weight ensures one-trial sequence learning of place fields in the hippocampus , 2006, Neural Networks.

[63]  U. Karmarkar,et al.  Different forms of homeostatic plasticity are engaged with distinct temporal profiles , 2006, The European journal of neuroscience.

[64]  Kamal Sen,et al.  Increasing Ca2+ transients by broadening postsynaptic action potentials enhances timing-dependent synaptic depression. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[65]  Cathryn L. Kubera,et al.  Astrocytic Purinergic Signaling Coordinates Synaptic Networks , 2005, Science.

[66]  R. Tsien,et al.  Adaptation to Synaptic Inactivity in Hippocampal Neurons , 2005, Neuron.

[67]  N. Spruston,et al.  Postsynaptic depolarization requirements for LTP and LTD: a critique of spike timing-dependent plasticity , 2005, Nature Neuroscience.

[68]  T. Sejnowski,et al.  Homeostatic synaptic plasticity can explain post-traumatic epileptogenesis in chronically isolated neocortex. , 2005, Cerebral cortex.

[69]  Y. Dan,et al.  Spike-timing-dependent synaptic plasticity depends on dendritic location , 2005, Nature.

[70]  Sen Song,et al.  Highly Nonrandom Features of Synaptic Connectivity in Local Cortical Circuits , 2005, PLoS biology.

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

[72]  Joseph E LeDoux,et al.  Heterosynaptic Long-Term Potentiation of Inhibitory Interneurons in the Lateral Amygdala , 2004, The Journal of Neuroscience.

[73]  L. Cooper,et al.  Synaptic homeostasis and input selectivity follow from a calcium-dependent plasticity model. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

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

[75]  D. Ulrich,et al.  Firing Mode-Dependent Synaptic Plasticity in Rat Neocortical Pyramidal Neurons , 2004, The Journal of Neuroscience.

[76]  M. Volgushev,et al.  Dependence of calcium influx in neocortical cells on temporal structure of depolarization, number of spikes, and blockade of NMDA receptors , 2004, Journal of neuroscience research.

[77]  Michael Häusser,et al.  A proportional but slower NMDA potentiation follows AMPA potentiation in LTP , 2004, Nature Neuroscience.

[78]  A. Peters,et al.  The selfish brain: competition for energy resources , 2004, Neuroscience & Biobehavioral Reviews.

[79]  Daniel Johnston,et al.  LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites , 2004, Nature Neuroscience.

[80]  S. Nelson,et al.  Homeostatic plasticity in the developing nervous system , 2004, Nature Reviews Neuroscience.

[81]  A. Zador,et al.  Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex , 2003, Nature.

[82]  D. Linden,et al.  The other side of the engram: experience-driven changes in neuronal intrinsic excitability , 2003, Nature Reviews Neuroscience.

[83]  V. Murthy,et al.  Synaptic gain control and homeostasis , 2003, Current Opinion in Neurobiology.

[84]  Bert Sakmann,et al.  Supralinear Ca2+ Influx into Dendritic Tufts of Layer 2/3 Neocortical Pyramidal Neurons In Vitro and In Vivo , 2003, The Journal of Neuroscience.

[85]  T. Freund,et al.  Role of endogenous cannabinoids in synaptic signaling. , 2003, Physiological reviews.

[86]  P. Castillo,et al.  Heterosynaptic LTD of Hippocampal GABAergic Synapses A Novel Role of Endocannabinoids in Regulating Excitability , 2003, Neuron.

[87]  Haim Sompolinsky,et al.  Learning Input Correlations through Nonlinear Temporally Asymmetric Hebbian Plasticity , 2003, The Journal of Neuroscience.

[88]  Maxim Volgushev,et al.  γ‐Frequency fluctuations of the membrane potential and response selectivity in visual cortical neurons , 2003, The European journal of neuroscience.

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

[90]  Wulfram Gerstner,et al.  Mathematical formulations of Hebbian learning , 2002, Biological Cybernetics.

[91]  V. Murthy,et al.  Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons , 2002, Nature.

[92]  Dominique Debanne,et al.  Bidirectional plasticity of excitatory postsynaptic potential (EPSP)-spike coupling in CA1 hippocampal pyramidal neurons , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[93]  Niraj S. Desai,et al.  Critical periods for experience-dependent synaptic scaling in visual cortex , 2002, Nature Neuroscience.

[94]  Nace L. Golding,et al.  Dendritic spikes as a mechanism for cooperative long-term potentiation , 2002, Nature.

[95]  T. Elliott,et al.  Multiplicative Synaptic Normalization and a Nonlinear Hebb Rule Underlie a Neurotrophic Model of Competitive Synaptic Plasticity , 2002, Neural Computation.

[96]  E. Speckmann,et al.  Synaptic transmission in rat hippocampal slices is modulated by melatonin in a diurnal manner , 2002 .

[97]  P. J. Sjöström,et al.  Rate, Timing, and Cooperativity Jointly Determine Cortical Synaptic Plasticity , 2001, Neuron.

[98]  Wulfram Gerstner,et al.  Intrinsic Stabilization of Output Rates by Spike-Based Hebbian Learning , 2001, Neural Computation.

[99]  T. Schikorski,et al.  Inactivity Produces Increases in Neurotransmitter Release and Synapse Size , 2001, Neuron.

[100]  P. De Camilli,et al.  Chronic Blockade of Glutamate Receptors Enhances Presynaptic Release and Downregulates the Interaction between Synaptophysin-Synaptobrevin–Vesicle-Associated Membrane Protein 2 , 2001, The Journal of Neuroscience.

[101]  R. Nicoll,et al.  Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses , 2001, Nature.

[102]  P. Haydon Glia: listening and talking to the synapse , 2001, Nature Reviews Neuroscience.

[103]  Mark C. W. van Rossum,et al.  Stable Hebbian Learning from Spike Timing-Dependent Plasticity , 2000, The Journal of Neuroscience.

[104]  M. Volgushev,et al.  Retrograde signalling with nitric oxide at neocortical synapses , 2000, The European journal of neuroscience.

[105]  M. Poo,et al.  Calcium stores regulate the polarity and input specificity of synaptic modification , 2000, Nature.

[106]  L. Abbott,et al.  Synaptic plasticity: taming the beast , 2000, Nature Neuroscience.

[107]  L. Abbott,et al.  Competitive Hebbian learning through spike-timing-dependent synaptic plasticity , 2000, Nature Neuroscience.

[108]  D. Feldman,et al.  Timing-Based LTP and LTD at Vertical Inputs to Layer II/III Pyramidal Cells in Rat Barrel Cortex , 2000, Neuron.

[109]  B. Sakmann,et al.  Calcium electrogenesis in distal apical dendrites of layer 5 pyramidal cells at a critical frequency of back-propagating action potentials. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[110]  M. Volgushev,et al.  Interaction between intracellular tetanization and pairing-induced long-term synaptic plasticity in the rat visual cortex , 1999, Neuroscience.

[111]  J. A. Varela,et al.  Differential Depression at Excitatory and Inhibitory Synapses in Visual Cortex , 1999, The Journal of Neuroscience.

[112]  R. Zucker,et al.  Selective induction of LTP and LTD by postsynaptic [Ca2+]i elevation. , 1999, Journal of neurophysiology.

[113]  G. Bi,et al.  Synaptic Modifications in Cultured Hippocampal Neurons: Dependence on Spike Timing, Synaptic Strength, and Postsynaptic Cell Type , 1998, The Journal of Neuroscience.

[114]  U. Frey,et al.  Synaptic tagging: implications for late maintenance of hippocampal long-term potentiation , 1998, Trends in Neurosciences.

[115]  H. Markram,et al.  Differential signaling via the same axon of neocortical pyramidal neurons. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[116]  Niraj S. Desai,et al.  Activity-dependent scaling of quantal amplitude in neocortical neurons , 1998, Nature.

[117]  Charles F Stevens,et al.  Synaptic plasticity , 1998, Current Biology.

[118]  L. Abbott,et al.  A Quantitative Description of Short-Term Plasticity at Excitatory Synapses in Layer 2/3 of Rat Primary Visual Cortex , 1997, The Journal of Neuroscience.

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

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

[121]  P. Schulz,et al.  Long-term potentiation involves increases in the probability of neurotransmitter release. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

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

[123]  H. Markram,et al.  The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[124]  L. Abbott,et al.  Synaptic Depression and Cortical Gain Control , 1997, Science.

[125]  H. Sompolinsky,et al.  Chaos in Neuronal Networks with Balanced Excitatory and Inhibitory Activity , 1996, Science.

[126]  K. Miller,et al.  Synaptic Economics: Competition and Cooperation in Synaptic Plasticity , 1996, Neuron.

[127]  H. Markram,et al.  Redistribution of synaptic efficacy between neocortical pyramidal neurons , 1996, Nature.

[128]  R. Zucker,et al.  Long-lasting potentiation and depression without presynaptic activity. , 1996, Journal of neurophysiology.

[129]  R. Nicoll,et al.  Ca2+ Signaling Requirements for Long-Term Depression in the Hippocampus , 1996, Neuron.

[130]  U. Staubli,et al.  The induction of homo- vs. heterosynaptic LTD in area CA1 of hippocampal slices from adult rats , 1996, Brain Research.

[131]  M. Bear,et al.  Metaplasticity: the plasticity of synaptic plasticity , 1996, Trends in Neurosciences.

[132]  Robert S. Zucker,et al.  Postsynaptic Levels of [Ca2+]i Needed to Trigger LTD and LTP , 1996, Neuron.

[133]  N. Spruston,et al.  Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. , 1995, Science.

[134]  W Singer,et al.  Induction of LTP and LTD in visual cortex neurones by intracellular tetanization , 1994, Neuroreport.

[135]  U. Kuhnt,et al.  Long term enhancement of synaptic transmission in the hippocampus after tetanization of single neurons by short intracellular current pulses , 1994 .

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

[137]  W. Singer,et al.  Long-term depression of excitatory synaptic transmission and its relationship to long-term potentiation , 1993, Trends in Neurosciences.

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

[139]  B. Gähwiler,et al.  Presynaptic inhibition of miniature excitatory synaptic currents by baclofen and adenosine in the hippocampus , 1992, Neuron.

[140]  B. Alger,et al.  Postsynaptic spike firing reduces synaptic GABAA responses in hippocampal pyramidal cells , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[141]  B. Gähwiler,et al.  Comparison of the actions of adenosine at pre‐ and postsynaptic receptors in the rat hippocampus in vitro. , 1992, The Journal of physiology.

[142]  R. Malenka,et al.  The influence of prior synaptic activity on the induction of long-term potentiation. , 1992, Science.

[143]  R. Malenka,et al.  Characterization of the integration time for the stabilization of long- term potentiation in area CA1 of the hippocampus , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[144]  R. H. White,et al.  Competitive Hebbian learning , 1991, IJCNN-91-Seattle International Joint Conference on Neural Networks.

[145]  M. Meltzer,et al.  Tumor necrosis factor. , 1991, Journal of the American Academy of Dermatology.

[146]  J. Bolz,et al.  Non-Hebbian synapses in rat visual cortex. , 1990, Neuroreport.

[147]  W B Levy,et al.  Spatial overlap between populations of synapses determines the extent of their associative interaction during the induction of long-term potentiation and depression. , 1990, Journal of neurophysiology.

[148]  C. Stevens,et al.  Presynaptic mechanism for long-term potentiation in the hippocampus , 1990, Nature.

[149]  J. Lisman,et al.  A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[150]  A. Aertsen,et al.  Synaptic plasticity in rat hippocampal slice cultures: local "Hebbian" conjunction of pre- and postsynaptic stimulation leads to distributed synaptic enhancement. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[151]  T. Dunwiddie,et al.  Adenosine increases synaptic facilitation in the in vitro rat hippocampus: evidence for a presynaptic site of action. , 1985, The Journal of physiology.

[152]  C. Blakemore,et al.  Development of orientation columns in cat striate cortex revealed by 2-deoxyglucose autoradiography , 1983, Nature.

[153]  E. Bienenstock,et al.  Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[155]  M M Merzenich,et al.  Representation of cochlea within primary auditory cortex in the cat. , 1975, Journal of neurophysiology.

[156]  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.

[157]  D. Anderson,et al.  Tonotopic organization and discharge characteristics of single neurons in nuclei of the lateral lemniscus of the cat. , 1970, Journal of neurophysiology.

[158]  D. Hubel,et al.  EFFECTS OF VISUAL DEPRIVATION ON MORPHOLOGY AND PHYSIOLOGY OF CELLS IN THE CATS LATERAL GENICULATE BODY. , 1963, Journal of neurophysiology.

[159]  C A Nelson,et al.  Learning to Learn , 2017, Encyclopedia of Machine Learning and Data Mining.

[160]  G. Turrigiano Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function. , 2012, Cold Spring Harbor perspectives in biology.

[161]  Gina G. Turrigiano,et al.  Homeostatic Synaptic Plasticity , 2008 .

[162]  Y. Dan,et al.  Spike timing-dependent plasticity: a Hebbian learning rule. , 2008, Annual review of neuroscience.

[163]  C. Malsburg Self-organization of orientation sensitive cells in the striate cortex , 2004, Kybernetik.

[164]  Wulfram Gerstner,et al.  Short-Term Synaptic Plasticity Orchestrates the Response of Pyramidal Cells and Interneurons to Population Bursts , 2005, Journal of Computational Neuroscience.

[165]  L. Bindman,et al.  Long-term depression at synapses in slices of rat hippocampus can be induced by bursts of postsynaptic activity , 2004, Experimental Brain Research.

[166]  L. Abbott,et al.  Synaptic computation , 2004, Nature.

[167]  W. Regehr,et al.  Short-term synaptic plasticity. , 2002, Annual review of physiology.

[168]  A. van Ooyen Competition in the development of nerve connections: a review of models. , 2001, Network.

[169]  Ruey-Beei Wu,et al.  Differential Signaling , 2000 .

[170]  Kenneth D. Miller,et al.  The Role of Constraints in Hebbian Learning , 1994, Neural Computation.

[171]  G Christofi,et al.  The postsynaptic induction of nonassociative long-term depression of excitatory synaptic transmission in rat hippocampal slices. , 1993, Journal of neurophysiology.

[172]  E. Oja Simplified neuron model as a principal component analyzer , 1982, Journal of mathematical biology.