Spatiotemporal specificity of synaptic plasticity: cellular rules and mechanisms

Abstract. Recent experimental results on spike-timing-dependent plasticity (STDP) and heterosynaptic interaction in various systems have revealed new temporal and spatial properties of activity-dependent synaptic plasticity. These results challenge the conventional understanding of Hebb's rule and raise intriguing questions regarding the fundamental processes of cellular signaling. In this article, I review these new findings that lead to formulation of a new set of cellular rules. Emphasis is on evaluating potential molecular and cellular mechanisms that may underlie the spike-timing window of STDP and different patterns of heterosynaptic modifications. I also highlight several unresolved issues, and suggest future lines of research.

[1]  M. Quirk,et al.  Experience-Dependent Asymmetric Shape of Hippocampal Receptive Fields , 2000, Neuron.

[2]  B. Gustafsson,et al.  Hippocampal long-lasting potentiation produced by pairing single volleys and brief conditioning tetani evoked in separate afferents , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  Dieter G. Weiss,et al.  Actin-dependent organelle movement in squid axoplasm , 1992, Nature.

[4]  K. Svoboda,et al.  Synaptic [Ca2+] Intracellular Stores Spill Their Guts , 1999, Neuron.

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

[6]  T. Sejnowski,et al.  Storing covariance with nonlinearly interacting neurons , 1977, Journal of mathematical biology.

[7]  Michele Migliore,et al.  Role of an A-Type K+ Conductance in the Back-Propagation of Action Potentials in the Dendrites of Hippocampal Pyramidal Neurons , 1999, Journal of Computational Neuroscience.

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

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

[10]  W. N. Ross,et al.  Imaging voltage and synaptically activated sodium transients in cerebellar Purkinje cells , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

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

[12]  S. Kelso,et al.  Hebbian synapses in hippocampus. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

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

[14]  M. Mayer,et al.  Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurones , 1984, Nature.

[15]  Y. Jan,et al.  Changing subunit composition of heteromeric NMDA receptors during development of rat cortex , 1994, Nature.

[16]  R. Kempter,et al.  Formation of temporal-feature maps by axonal propagation of synaptic learning , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[17]  K. Williams,et al.  Developmental switch in the expression of NMDA receptors occurs in vivo and in vitro , 1993, Neuron.

[18]  R. Dolmetsch,et al.  Signaling to the Nucleus by an L-type Calcium Channel-Calmodulin Complex Through the MAP Kinase Pathway , 2001, Science.

[19]  Daniel Johnston,et al.  Multiple forms of LTP in hippocampal CA3 neurons use a common postsynaptic mechanism , 1999, Nature Neuroscience.

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

[21]  E. Rolls,et al.  Neural networks and brain function , 1998 .

[22]  P. De Koninck,et al.  Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations. , 1998, Science.

[23]  M. Yeckel,et al.  Hippocampal mossy fiber activity evokes Ca2+ release in CA3 pyramidal neurons via a metabotropic glutamate receptor pathway , 2001, Neuroscience.

[24]  A. Konnerth,et al.  Sodium action potentials in the dendrites of cerebellar Purkinje cells. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[25]  G. Buzsáki,et al.  Pattern and inhibition-dependent invasion of pyramidal cell dendrites by fast spikes in the hippocampus in vivo. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Geoffrey E. Hinton,et al.  Learning representations by back-propagation errors, nature , 1986 .

[27]  M Migliore,et al.  Dendritic potassium channels in hippocampal pyramidal neurons , 2000, The Journal of physiology.

[28]  Henry Markram,et al.  An Algorithm for Modifying Neurotransmitter Release Probability Based on Pre- and Postsynaptic Spike Timing , 2001, Neural Computation.

[29]  R. Nicoll,et al.  Neurobiology: Long-distance long-term depression , 1997, Nature.

[30]  G. Bloom,et al.  Mechanisms of fast and slow axonal transport. , 1991, Annual review of neuroscience.

[31]  Davide Badoni,et al.  Spike-Driven Synaptic Plasticity: Theory, Simulation, VLSI Implementation , 2000, Neural Computation.

[32]  Li I. Zhang,et al.  A critical window for cooperation and competition among developing retinotectal synapses , 1998, Nature.

[33]  R. Nicoll,et al.  An essential role for postsynaptic calmodulin and protein kinase activity in long-term potentiation , 1989, Nature.

[34]  T. Sejnowski,et al.  The Book of Hebb , 1999, Neuron.

[35]  Guo-Qiang Bi,et al.  Kinesin- and Myosin-driven Steps of Vesicle Recruitment for Ca2+-regulated Exocytosis , 1997, The Journal of cell biology.

[36]  F. Crépel,et al.  Homo‐ and heterosynaptic changes in efficacy are expressed in prefrontal neurons: An in vitro study in the rat , 1992, Synapse.

[37]  S. Vicini,et al.  Functional and pharmacological differences between recombinant N-methyl-D-aspartate receptors. , 1998, Journal of neurophysiology.

[38]  W. Levy,et al.  Temporal contiguity requirements for long-term associative potentiation/depression in the hippocampus , 1983, Neuroscience.

[39]  J. Connor,et al.  Dendritic spines as individual neuronal compartments for synaptic Ca2+ responses , 1991, Nature.

[40]  N J Emptage,et al.  Long-term synaptic facilitation in the absence of short-term facilitation in Aplysia neurons. , 1993, Science.

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

[42]  Florian Engert,et al.  Emergence of Input Specificity of LTP during Development of Retinotectal Connections In Vivo , 2001, Neuron.

[43]  Mark Farrant,et al.  NMDA receptor subunits: diversity, development and disease , 2001, Current Opinion in Neurobiology.

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

[45]  Arthur Konnerth,et al.  Early postnatal switch in magnesium sensitivity of NMDA receptors in rat CA1 pyramidal cells , 1999, The Journal of physiology.

[46]  W. Levy,et al.  Synapses as associative memory elements in the hippocampal formation , 1979, Brain Research.

[47]  B. Sakmann,et al.  Calcium dynamics in single spines during coincident pre- and postsynaptic activity depend on relative timing of back-propagating action potentials and subthreshold excitatory postsynaptic potentials. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[48]  E. D’Angelo,et al.  Beyond parallel fiber LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum , 2001, Nature Neuroscience.

[49]  R. Hawkins,et al.  Nitric oxide as a retrograde messenger during long-term potentiation in hippocampus. , 1998, Progress in brain research.

[50]  Y. Dan,et al.  Stimulus Timing-Dependent Plasticity in Cortical Processing of Orientation , 2001, Neuron.

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

[52]  D. Johnston,et al.  Active properties of neuronal dendrites. , 1996, Annual review of neuroscience.

[53]  Patrick D. Roberts,et al.  Computational Consequences of Temporally Asymmetric Learning Rules: I. Differential Hebbian Learning , 1999, Journal of Computational Neuroscience.

[54]  V. Han,et al.  Synaptic plasticity in a cerebellum-like structure depends on temporal order , 1997, Nature.

[55]  G. Bi,et al.  Distributed synaptic modification in neural networks induced by patterned stimulation , 1999, Nature.

[56]  G. Stent A physiological mechanism for Hebb's postulate of learning. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[57]  George Kunos,et al.  Presynaptic Specificity of Endocannabinoid Signaling in the Hippocampus , 2001, Neuron.

[58]  Michael P. Sheetz,et al.  Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility , 1985, Cell.

[59]  D. Debanne,et al.  Long‐term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures , 1998, The Journal of physiology.

[60]  Li I. Zhang,et al.  Selective Presynaptic Propagation of Long-Term Potentiation in Defined Neural Networks , 2000, The Journal of Neuroscience.

[61]  G. A. Clark,et al.  Induction of long-term facilitation in Aplysia sensory neurons by local application of serotonin to remote synapses. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[62]  R. Malenka,et al.  Involvement of a calcineurin/ inhibitor-1 phosphatase cascade in hippocampal long-term depression , 1994, Nature.

[63]  Y. Dan,et al.  Spike-timing-dependent synaptic modification induced by natural spike trains , 2002, Nature.

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

[65]  M. Berridge Neuronal Calcium Signaling , 1998, Neuron.

[66]  V. Han,et al.  Reversible Associative Depression and Nonassociative Potentiation at a Parallel Fiber Synapse , 2000, Neuron.

[67]  M. Poo,et al.  Long-range signaling in growing neurons after local elevation of cyclic AMP-dependent activity , 1994, The Journal of cell biology.

[68]  R. Tsien,et al.  Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP. , 1989, Science.

[69]  M. Poo,et al.  Spread of Synaptic Depression Mediated by Presynaptic Cytoplasmic Signaling , 1996, Science.

[70]  Terrence J. Sejnowski,et al.  The Hebb Rule for Synaptic Plasticity: Algorithms and Implementations , 1989 .

[71]  L. Abbott,et al.  Cortical Development and Remapping through Spike Timing-Dependent Plasticity , 2001, Neuron.

[72]  R. Zucker Calcium- and activity-dependent synaptic plasticity , 1999, Current Opinion in Neurobiology.

[73]  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.

[74]  H. Markram,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997, Science.

[75]  D. Linden,et al.  Long-term synaptic depression. , 1995, Annual review of neuroscience.

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

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

[78]  H. Monyer,et al.  NR2A Subunit Expression Shortens NMDA Receptor Synaptic Currents in Developing Neocortex , 1997, The Journal of Neuroscience.

[79]  M. Sheng,et al.  PDZ domains and the organization of supramolecular complexes. , 2001, Annual review of neuroscience.

[80]  Richard L. Huganir,et al.  Postsynaptic organisation and regulation of excitatory synapses , 2000, Nature Reviews Neuroscience.

[81]  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.

[82]  H. Wigström,et al.  Hippocampal long-term potentiation is induced by pairing single afferent volleys with intracellularly injected depolarizing current pulses. , 1986, Acta physiologica Scandinavica.

[83]  A. C. Greenwood,et al.  Bidirectional synaptic plasticity correlated with the magnitude of dendritic calcium transients above a threshold. , 2001, Journal of neurophysiology.

[84]  B. Sakmann,et al.  Developmental and regional expression in the rat brain and functional properties of four NMDA receptors , 1994, Neuron.

[85]  Rajesh P. N. Rao,et al.  Spike-Timing-Dependent Hebbian Plasticity as Temporal Difference Learning , 2001, Neural Computation.

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

[87]  J. Sarvey,et al.  Heterosynaptic postactivation potentiation in hippocampal CA 3 neurons: Long-term changes of the postsynaptic potentials , 1979, Experimental Brain Research.

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

[89]  Louis J Muglia,et al.  Calcium-Stimulated Adenylyl Cyclase Activity Is Critical for Hippocampus-Dependent Long-Term Memory and Late Phase LTP , 1999, Neuron.

[90]  Charles F Stevens,et al.  Long-Term Depression Properties in a Simple System , 1996, Neuron.

[91]  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.

[92]  Wulfram Gerstner,et al.  Learning Navigational Maps Through Potentiation and Modulation of Hippocampal Place Cells , 2004, Journal of Computational Neuroscience.

[93]  A. Konnerth,et al.  Stores Not Just for Storage Intracellular Calcium Release and Synaptic Plasticity , 2001, Neuron.

[94]  M. Poo,et al.  Retrograde signaling at central synapses , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[95]  B. Sakmann,et al.  Active propagation of somatic action potentials into neocortical pyramidal cell dendrites , 1994, Nature.

[96]  B. McNaughton,et al.  Experience-dependent, asymmetric expansion of hippocampal place fields. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[97]  G. V. Goddard,et al.  Asymmetric relationships between homosynaptic long-term potentiation and heterosynaptic long-term depression , 1983, Nature.

[98]  M. Bear,et al.  Long-term depression in hippocampus. , 1996, Annual review of neuroscience.

[99]  R. Malenka,et al.  Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus , 1992, Neuron.

[100]  T. Tsumoto,et al.  Evidence for excitatory connections from the deprived eye to the visual cortex in monocularly deprived kittens , 1978, Brain Research.

[101]  W. Denk,et al.  Dendritic spines as basic functional units of neuronal integration , 1995, Nature.

[102]  L. Nowak,et al.  Magnesium gates glutamate-activated channels in mouse central neurones , 1984, Nature.

[103]  Roberto Malinow,et al.  LTP mechanisms: from silence to four-lane traffic , 2000, Current Opinion in Neurobiology.

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

[105]  R. Nicoll,et al.  Mechanisms underlying long-term potentiation of synaptic transmission. , 1991, Annual review of neuroscience.

[106]  M. Bear,et al.  Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

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

[108]  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.

[109]  E. Kandel,et al.  Toward a molecular definition of long-term memory storage. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[110]  Guo-Qiang Bi,et al.  Synaptic modification in neural circuits: a timely action. , 2002, BioEssays : news and reviews in molecular, cellular and developmental biology.

[111]  E. W. Kairiss,et al.  Hebbian synapses: biophysical mechanisms and algorithms. , 1990, Annual review of neuroscience.

[112]  G. Barrionuevo,et al.  Long‐term potentiation in hippocampal CA3 neurons: Tetanized input regulates heterosynaptic efficacy , 1989, Synapse.

[113]  A. West,et al.  Calcium regulation of neuronal gene expression , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[114]  Arthur Konnerth,et al.  Calcium and Activity-Dependent Synaptic Plasticity , 1998 .

[115]  E Neher,et al.  Usefulness and limitations of linear approximations to the understanding of Ca++ signals. , 1998, Cell calcium.

[116]  Martin Schneider,et al.  Activity-Dependent Development of Axonal and Dendritic Delays, or, Why Synaptic Transmission Should Be Unreliable , 2002, Neural Computation.

[117]  S. Shenolikar,et al.  Gating of CaMKII by cAMP-regulated protein phosphatase activity during LTP. , 1998, Science.

[118]  K. Mikoshiba,et al.  Facilitation of NMDAR-Independent LTP and Spatial Learning in Mutant Mice Lacking Ryanodine Receptor Type 3 , 1999, Neuron.

[119]  Wulfram Gerstner,et al.  A neuronal learning rule for sub-millisecond temporal coding , 1996, Nature.

[120]  Geoffrey E. Hinton,et al.  Learning representations by back-propagating errors , 1986, Nature.

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

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

[123]  T. Bonhoeffer,et al.  Pairing-Induced Changes of Orientation Maps in Cat Visual Cortex , 2001, Neuron.

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

[125]  A. Ganong,et al.  Excitatory amino acid neurotransmission: NMDA receptors and Hebb-type synaptic plasticity. , 1988, Annual review of neuroscience.

[126]  M. W. Brown,et al.  An experimental test of the role of postsynaptic calcium levels in determining synaptic strength using perirhinal cortex of rat , 2001, The Journal of physiology.

[127]  B. Sakmann,et al.  Coincidence detection and changes of synaptic efficacy in spiny stellate neurons in rat barrel cortex , 1999, Nature Neuroscience.

[128]  M. Poo,et al.  Propagation of activity-dependent synaptic depression in simple neural networks , 1997, Nature.

[129]  P. Andersen,et al.  Specific long-lasting potentiation of synaptic transmission in hippocampal slices , 1977, Nature.

[130]  K. Svoboda,et al.  Structure and function of dendritic spines. , 2002, Annual review of physiology.

[131]  Allen I. Selverston,et al.  Spatio-temporal dynamics of cyclic AMP signals in an intact neural circuit , 1996, Nature.

[132]  D. Muller,et al.  Heterosynaptic interactions between UP and LTD in CA1 hippocampal slices , 1995, Neuron.

[133]  K. I. Blum,et al.  Functional significance of long-term potentiation for sequence learning and prediction. , 1996, Cerebral cortex.

[134]  J. Kauer,et al.  Hippocampal Interneurons Express a Novel Form of Synaptic Plasticity , 1997, Neuron.

[135]  W. Singer,et al.  Relation Between Dendritic Ca2+ Levels and the Polarity of Synaptic Long‐term Modifications in Rat Visual Cortex Neurons , 1997, The European journal of neuroscience.

[136]  K. Deisseroth,et al.  Translocation of calmodulin to the nucleus supports CREB phosphorylation in hippocampal neurons , 1998, Nature.

[137]  B. R. Sastry,et al.  Associative induction of posttetanic and long-term potentiation in CA1 neurons of rat hippocampus. , 1986, Science.

[138]  K. Deisseroth,et al.  L-type calcium channels and GSK-3 regulate the activity of NF-ATc4 in hippocampal neurons , 1999, Nature.

[139]  Daniel D. Lee,et al.  Equilibrium properties of temporally asymmetric Hebbian plasticity. , 2000, Physical review letters.

[140]  G. Lynch,et al.  Long‐term potentiation and depression of synaptic responses in the rat hippocampus: localization and frequency dependency. , 1978, The Journal of physiology.

[141]  R. Kempter,et al.  Hebbian learning and spiking neurons , 1999 .

[142]  W. N. Ross,et al.  Synergistic Release of Ca2+ from IP3-Sensitive Stores Evoked by Synaptic Activation of mGluRs Paired with Backpropagating Action Potentials , 1999, Neuron.

[143]  B. Berninger,et al.  Neurotrophins and activity-dependent plasticity of cortical interneurons , 1997, Trends in Neurosciences.

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

[145]  S. Redman,et al.  Long-term plasticity at excitatory synapses on aspinous interneurons in area CA1 lacks synaptic specificity. , 1998, Journal of neurophysiology.

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