Homeostatic plasticity in the CNS: synaptic and intrinsic forms

The study of experience-dependent plasticity has been dominated by questions of how Hebbian plasticity mechanisms act during learning and development. This is unsurprising as Hebbian plasticity constitutes the most fully developed and influential model of how information is stored in neural circuits and how neural circuitry can develop without extensive genetic instructions. Yet Hebbian plasticity may not be sufficient for understanding either learning or development: the dramatic changes in synapse number and strength that can be produced by this kind of plasticity tend to threaten the stability of neural circuits. Recent work has suggested that, in addition to Hebbian plasticity, homeostatic regulatory mechanisms are active in a variety of preparations. These mechanisms alter both the synaptic connections between neurons and the intrinsic electrical properties of individual neurons, in such a way as to maintain some constancy in neuronal properties despite the changes wrought by Hebbian mechanisms. Here we review the evidence for homeostatic plasticity in the central nervous system, with special emphasis on results from cortical preparations.

[1]  Jian Wang,et al.  CaMKII regulates the frequency-response function of hippocampal synapses for the production of both LTD and LTP , 1995, Cell.

[2]  G. Bi,et al.  Synaptic modification by correlated activity: Hebb's postulate revisited. , 2001, Annual review of neuroscience.

[3]  R. Nicoll,et al.  Activity differentially regulates the surface expression of synaptic AMPA and NMDA glutamate receptors. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Nathan Intrator,et al.  Solutions of the BCM learning rule in a network of lateral interacting nonlinear neurons , 1999 .

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

[6]  D. Hubel,et al.  The period of susceptibility to the physiological effects of unilateral eye closure in kittens , 1970, The Journal of physiology.

[7]  M. V. Rossum,et al.  Activity Coregulates Quantal AMPA and NMDA Currents at Neocortical Synapses , 2000, Neuron.

[8]  J. Lichtman,et al.  Alterations in Synaptic Strength Preceding Axon Withdrawal , 1997, Science.

[9]  W. Cannon,et al.  A LAW OF DENERVATION , 1939 .

[10]  S. Hoffman,et al.  Funding for malaria genome sequencing , 1997, Nature.

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

[12]  S. Nelson,et al.  BDNF Has Opposite Effects on the Quantal Amplitude of Pyramidal Neuron and Interneuron Excitatory Synapses , 1998, Neuron.

[13]  D. Johnston,et al.  A Synaptically Controlled, Associative Signal for Hebbian Plasticity in Hippocampal Neurons , 1997, Science.

[14]  Eytan Domany,et al.  Models of Neural Networks I , 1991 .

[15]  Niraj S. Desai,et al.  Plasticity in the intrinsic excitability of cortical pyramidal neurons , 1999, Nature Neuroscience.

[16]  G. Turrigiano Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same , 1999, Trends in Neurosciences.

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

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

[19]  T. Nick,et al.  Synaptic activity modulates presynaptic excitability , 2000, Nature Neuroscience.

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

[21]  L. Ballerini,et al.  Homeostatic plasticity induced by chronic block of AMPA/kainate receptors modulates the generation of rhythmic bursting in rat spinal cord organotypic cultures , 2001, The European journal of neuroscience.

[22]  K. Fox,et al.  A critical period for experience-dependent synaptic plasticity in rat barrel cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[24]  E. D'Angelo,et al.  Long-Term Potentiation of Intrinsic Excitability at the Mossy Fiber–Granule Cell Synapse of Rat Cerebellum , 2000, The Journal of Neuroscience.

[25]  E Marder,et al.  Memory from the dynamics of intrinsic membrane currents. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Sacha B. Nelson,et al.  Activity-dependent regulation of excitability in rat visual cortical neurons , 1999, Neurocomputing.

[27]  A. L. Willard,et al.  Long-term regulation of neuronal calcium currents by prolonged changes of membrane potential , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  G. Davis,et al.  Maintaining the stability of neural function: a homeostatic hypothesis. , 2001, Annual review of physiology.

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

[30]  K. Miller Receptive Fields and Maps in the Visual Cortex: Models of Ocular Dominance and Orientation Columns* , 1996 .

[31]  Mark F. Bear,et al.  Heterosynaptic metaplasticity in the hippocampus in vivo: A BCM-like modifiable threshold for LTP , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[32]  E. Marder,et al.  Activity-Dependent Regulation of Potassium Currents in an Identified Neuron of the Stomatogastric Ganglion of the Crab Cancer borealis , 1999, The Journal of Neuroscience.

[33]  Peter Dayan,et al.  Theoretical Neuroscience: Computational and Mathematical Modeling of Neural Systems , 2001 .

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

[35]  Johan F. Storm,et al.  Temporal integration by a slowly inactivating K+ current in hippocampal neurons , 1988, Nature.

[36]  E. Marder,et al.  Activity-dependent changes in the intrinsic properties of cultured neurons. , 1994, Science.

[37]  William Wisden,et al.  Adaptive regulation of neuronal excitability by a voltage- independent potassium conductance , 2001, Nature.

[38]  R. Huganir,et al.  Activity-Dependent Modulation of Synaptic AMPA Receptor Accumulation , 1998, Neuron.

[39]  E. Marder,et al.  Activity-dependent regulation of conductances in model neurons. , 1993, Science.

[40]  D. Johnston,et al.  K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons , 1997, Nature.

[41]  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.

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

[43]  S. Sampson,et al.  Characterization of the relation between sodium channels and electrical activity in cultured rat skeletal myotubes: regulatory aspects , 1989, Brain Research.

[44]  Joseph E LeDoux,et al.  Fear conditioning induces associative long-term potentiation in the amygdala , 1997, Nature.

[45]  M. Bear,et al.  Experience-dependent modification of synaptic plasticity in visual cortex , 1996, Nature.

[46]  M. Bear,et al.  Synaptic plasticity: LTP and LTD , 1994, Current Opinion in Neurobiology.

[47]  E. Marder,et al.  Selective regulation of current densities underlies spontaneous changes in the activity of cultured neurons , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[48]  P G Nelson,et al.  Modulation of calcium currents by electrical activity. , 1996, Journal of neurophysiology.

[49]  H Wang,et al.  Priming-induced shift in synaptic plasticity in the rat hippocampus. , 1999, Journal of neurophysiology.

[50]  Mark C. W. van Rossum,et al.  Activity Deprivation Reduces Miniature IPSC Amplitude by Decreasing the Number of Postsynaptic GABAA Receptors Clustered at Neocortical Synapses , 2002, The Journal of Neuroscience.

[51]  M. Poo,et al.  Enhancement of presynaptic neuronal excitability by correlated presynaptic and postsynaptic spiking , 2000, Nature Neuroscience.

[52]  L. Cooper,et al.  Synaptic plasticity in visual cortex: comparison of theory with experiment. , 1991, Journal of neurophysiology.

[53]  M. Bear,et al.  Visual Experience and Deprivation Bidirectionally Modify the Composition and Function of NMDA Receptors in Visual Cortex , 2001, Neuron.

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

[55]  D. Linden,et al.  Rapid, synaptically driven increases in the intrinsic excitability of cerebellar deep nuclear neurons , 2000, Nature Neuroscience.

[56]  Niraj S. Desai,et al.  BDNF regulates the intrinsic excitability of cortical neurons. , 1999, Learning & memory.

[57]  G G Turrigiano,et al.  Brain-Derived Neurotrophic Factor Mediates the Activity-Dependent Regulation of Inhibition in Neocortical Cultures , 1997, The Journal of Neuroscience.

[58]  M. Poo,et al.  Activity-dependent synaptic competition in vitro: heterosynaptic suppression of developing synapses. , 1991, Science.

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

[60]  W. Abraham,et al.  Metaplasticity: A new vista across the field of synaptic plasticity , 1997, Progress in Neurobiology.

[61]  J. Donoghue,et al.  Learning-induced LTP in neocortex. , 2000, Science.

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

[63]  M. Corner,et al.  Activity-dependent plasticity of inhibitory and excitatory amino acid transmitter systems in cultured rat cerebral cortex , 1994, International Journal of Developmental Neuroscience.

[64]  J. Wagner,et al.  Primed Facilitation of Homosynaptic Long-Term Depression and Depotentiation in Rat Hippocampus , 1998, The Journal of Neuroscience.

[65]  C. Goodman,et al.  Synapse-specific control of synaptic efficacy at the terminals of a single neuron , 1998, Nature.

[66]  Z. Gil,et al.  Evidence for proportional synaptic scaling in neocortex of intact animals , 2000, Neuroreport.

[67]  S. Sharpless REORGANIZATION OF FUNCTION IN THE NERVOUS SYSTEM--USE AND DISUSE. , 1964, Annual review of physiology.