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Experimental and computational aspects of signaling mechanisms of spike‐timing‐dependent plasticity

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Pages 240-254 | Received 05 Dec 2008, Accepted 27 Apr 2009, Published online: 07 Sep 2010

References

  • Abbott , LF and Nelson , SB . 2000 . “Synaptic plasticity: taming the beast.” . Nat. Neurosci , 3 : 1178 – 1183 .
  • Ashby , MC , De La Rue , SA , Ralph , GS , Uney , J , Collingridge , GL and Henley , JM . 2004 . “Removal of AMPA receptors (AMPARs) from synapses is preceded by transient endocytosis of extrasynaptic AMPARs.” . J. Neurosci. , 24 : 5172 – 5176 .
  • Banke , TG , Bowie , D , Lee , H , Huganir , RL , Schousboe , A and Traynelis , SF . 2000 . “Control of GluR1 AMPA receptor function by cAMP‐dependent protein kinase.” . J. Neurosci. , 20 : 89 – 102 .
  • Barria , A , Muller , D , Derkach , V , Griffith , LC and Soderling , TR . 1997 . “Regulatory phosphorylation of AMPA‐type glutamate receptors by CaM‐KII during long‐term potentiation.” . Science , 276 : 2042 – 2045 .
  • Bastrikova , N , Gardner , GA , Reece , JM , Jeromin , A and Dudek , SM . 2008 . “Synapse elimination accompanies functional plasticity in hippocampal neurons.” . Proc. Natl. Acad. Sci. U.S.A. , 105 : 3123 – 3127 .
  • Beattie , EC , Carroll , RC , Yu , X , Morishita , W , Yasuda , H , von Zastrow , M and Malenka , RC . 2000 . “Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD.” . Nat. Neurosci. , 3 : 1291 – 1300 .
  • Bender , VA , Bender , KJ , Brasier , DJ and Feldman , DE . 2006 . “Two coincidence detectors for spike timing‐dependent plasticity in somatosensory cortex.” . J. Neurosci. , 26 : 4166 – 4177 .
  • Benke , TA , Lüthi , A , Isaac , JTR and Collingridge , GL . 1998 . “Modulation of AMPA receptor unitary conductance by synaptic activity.” . Nature London , 393 : 793 – 797 .
  • Bhalla , US and Iyengar , R . 1999 . “Emergent properties of networks of biological signaling pathways.” . Science , 283 : 381 – 387 .
  • Bi , GQ and Poo , MM . 1998 . “Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type.” . J. Neurosci. , 18 : 10464 – 10472 .
  • Bi , GQ and Wang , HX . 2002 . “Temporal asymmetry in spike timing‐dependent synaptic plasticity.” . Physiol. Behav. , 77 : 551 – 555 .
  • Blitzer , RD . 2005 . “Long‐term potentiation: mechanisms of induction and maintenance.” . Sci. STKE , 2005 : tr26
  • Bradshaw , JM , Kubota , Y , Meyer , T and Schulman , H . 2003 . “An ultrasensitive Ca2+/calmodulin‐dependent protein kinase II‐protein phosphatase 1 switch facilitates specificity in postsynaptic calcium signaling.” . Proc. Natl. Acad. Sci. U.S.A. , 100 : 10512 – 10517 .
  • Brasier , DJ and Feldman , DE . 2008 . “Synapse‐specific expression of functional presynaptic NMDA receptors in rat somatosensory cortex.” . J. Neurosci. , 28 : 2199 – 2211 .
  • Caporale , N and Dan , Y . 2008 . “Spike timing‐dependent plasticity: a Hebbian learning rule.” . Annu. Rev. Neurosci. , 31 : 25 – 46 .
  • Carlisle , HJ , Fink , AE , Grant , SG and O'Dell , TJ . 2008 . “Opposing effects of PSD‐93 and PSD‐95 on long‐term potentiation and spike timing‐dependent plasticity.” . J. Physiol. , 586 : 5885 – 5900 .
  • Cassenaer , S and Laurent , G . 2007 . “Hebbian STDP in mushroom bodies facilitates the synchronous flow of olfactory information in locusts.” . Nature London , 448 : 709 – 713 .
  • Cateau , H and Fukai , T . 2003 . “A stochastic method to predict the consequence of arbitrary forms of spike‐timing‐dependent plasticity.” . Neural Comput. , 15 : 597 – 620 .
  • Celikel , T , Szostak , VA and Feldman , DE . 2004 . “Modulation of spike timing by sensory deprivation during induction of cortical map plasticity.” . Nat. Neurosci. , 7 : 534 – 541 .
  • Cingolani , LA and Goda , Y . 2008 . “Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy.” . Nat. Rev. Neurosci. , 9 : 344 – 356 .
  • Corlew , R , Brasier , DJ , Feldman , DE and Philpot , BD . 2008 . “Presynaptic NMDA receptors: newly appreciated roles in cortical synaptic function and plasticity.” . Neuroscientist , 14 : 609 – 625 .
  • Corlew , R , Wang , Y , Ghermazien , H , Erisir , A and Philpot , BD . 2007 . “Developmental switch in the contribution of presynaptic and postsynaptic NMDA receptors to long‐term depression.” . J. Neurosci. , 27 : 9835 – 9845 .
  • Cousin , MA and Robinson , PJ . 2001 . “The dephosphins: dephosphorylation by calcineurin triggers synaptic vesicle endocytosis.” . Trends Neurosci. , 24 : 659 – 665 .
  • Dahmen , JC , Hartley , DE and King , AJ . 2008 . “Stimulus‐timing‐dependent plasticity of cortical frequency representation.” . J. Neurosci. , 28 : 13629 – 13639 .
  • Dan , Y and Poo , MM . 2006 . “Spike timing‐dependent plasticity: from synapse to perception.” . Physiol Rev. , 86 : 1033 – 1048 .
  • Debanne , D , Gahwiler , BH and Thompson , SM . 1998 . “Long‐term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures.” . J. Physiol. , 507 (Pt 1) : 237 – 247 .
  • Delord , B , Berry , H , Guigon , E and Genet , S . 2007 . “A new principle for information storage in an enzymatic pathway model.” . PLOS Comput. Biol. , 3 : 1123 – 1135 .
  • Destexhe , A , Rudolph , M and Pare , D . 2003 . “The high‐conductance state of neocortical neurons in vivo.” . Nat. Rev. Neurosci. , 4 : 739 – 751 .
  • Duguid , I and Sjostrom , PJ . 2006 . “Novel presynaptic mechanisms for coincidence detection in synaptic plasticity.” . Curr. Opin. Neurobiol. , 16 : 312 – 322 .
  • Dupont , G , Houart , G and De Koninck, , P . 2003 . “Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations: a simple model.” . Cell Calcium , 34 : 485 – 497 .
  • Ehlers , MD , Heine , M , Groc , L , Lee , MC and Choquet , D . 2007 . “Diffusional trapping of GluR1 AMPA receptors by input‐specific synaptic activity.” . Neuron , 54 : 447 – 460 .
  • Ehlers , MD , Zhang , S , Bernhadt , JP and Huganir , RL . 1996 . “Inactivation of NMDA receptors by direct interaction of calmodulin with the NR1 subunit.” . Cell , 84 : 745 – 755 .
  • Engert , F , Tao , HW , Zhang , LI and Poo , MM . 2002 . “Moving visual stimuli rapidly induce direction sensitivity of developing tectal neurons.” . Nature London , 419 : 470 – 475 .
  • Feldman , DE . 2000 . “Timing‐based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex.” . Neuron , 27 : 45 – 56 .
  • Froemke , RC and Dan , Y . 2002 . “Spike‐timing‐dependent synaptic modification induced by natural spike trains.” . Nature London , 416 : 433 – 438 .
  • Froemke , RC , Poo , MM and Dan , Y . 2005 . “Spike‐timing‐dependent synaptic plasticity depends on dendritic location.” . Nature London , 434 : 221 – 225 .
  • Froemke , RC , Tsay , IA , Raad , M , Long , JD and Dan , Y . 2006 . “Contribution of individual spikes in burst‐induced long‐term synaptic modification.” . J. Neurophysiol. , 95 : 1620 – 1629 .
  • Fu , YX , Djupsund , K , Gao , H , Hayden , B , Shen , K and Dan , Y . 2002 . “Temporal specificity in the cortical plasticity of visual space representation.” . Science , 296 : 1999 – 2003 .
  • Fuenzalida , M , Fernandez de Sevilla , D and Buno , W . 2007 . “Changes of the EPSP waveform regulate the temporal window for spike‐timing‐dependent plasticity.” . J. Neurosci. , 11 : 11940 – 11948 .
  • Fukunaga , K , Stoppini , L , Miyamoto , E and Muller , D . 1993 . “Long‐term potentiation is associated with an increased activity of Ca2+/calmodulin‐dependent protein kinase II.” . J. Biol. Chem. , 268 : 7863 – 7867 .
  • Golding , NL , Staff , NP and Spruston , N . 2002 . “Dendritic spikes as a mechanism for cooperative long‐term potentiation.” . Nature London , 418 : 326 – 331 .
  • Gordon , U , Polsky , A and Schiller , J . 2006 . “Plasticity compartments in basal dendrites of neocortical pyramidal neurons.” . J. Neurosci. , 26 : 12717 – 12726 .
  • Graupner , M and Brunei , N . 2007 . “STDP in a bistable synapse model based on CaMKII and associated signaling pathways.” . PLOS Comput. Biol. , 3 : 2299 – 2323 .
  • Hanson , PI , Meyer , T , Stryer , L and Schulman , H . 1994 . “Dual role of calmodulin in autophosphorylation of multifunctional CaM kinase may underlie decoding of calcium signals.” . Neuron , 12 : 943 – 956 .
  • Hardie , J and Spruston , N . 2009 . “Synaptic depolarization is more effective than back‐propagating action potentials during induction of associative long‐term potentiation in hippocampal pyramidal neurons.” . J. Neurosci. , 29 : 3233 – 3241 .
  • Hashimotodani , Y , Ohno‐Shosaku , T and Kano , M . 2007 . “Ca2+‐assisted receptor‐driven endocannabinoid release: mechanisms that associate presynaptic and postsynaptic activities.” . Curr. Opin. Neurobiol. , 17 : 360 – 365 .
  • Hashimotodani , Y , Ohno‐Shosaku , T , Tsubokawa , H , Ogata , H , Emoto , K , Maejima , T , Araishi , K , Shin , HS and Kano , M . 2005 . “Phospholipase Cβ serves as a coincidence detector through its Ca2+ dependency for triggering retrograde endocannabinoid signal.” . Neuron , 45 : 257 – 268 .
  • Hayashi , Y , Shi , SH , Esteban , JA , Piccini , A , Poncer , JC and Malinow , R . 2000 . “Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluRl and PDZ domain interaction.” . Science , 287 : 2262 – 2267 .
  • Hayer , A and Bhalla , US . 2005 . “Molecular switches at the synapse emerge from receptor and kinase traffic.” . PLOS Comput. Biol. , 1 : 137 – 154 .
  • Hebb , D . 1949 . The Organization of Behavior, , New York : Wiley .
  • Helmchen , F . 2002 . “Raising the speed limit—fast Ca2+ handling in dendritic spines.” . Trends Neurosci. , 25 : 438 – 441 . 441
  • Hesse , GW and Teyler , TJ . 1976 . “Reversible loss of hippocampal long term potentiation following electroconvulsive seizures.” . Nature London , 264 : 562 – 564 .
  • Heynen , AJ , Quinlan , EM , Bae , DC and Bear , MF . 2000 . “Bidirectional, activity‐dependent regulation of glutamate receptors in the adult hippocampus in vivo.” . Neuron , 28 : 527 – 536 .
  • Hoffman , DA , Magee , JC , Colbert , CM and Johnston , D . 1997 . “K+channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons.” . Nature London , 387 : 869 – 875 .
  • Huang , CC , Liang , YC and Hsu , KS . 2001 . “Characterization of the mechanism underlying the reversal of long term potentiation by low frequency stimulation at hippocampal CA1 synapses.” . J. Biol. Chem. , 276 : 48108 – 48117 .
  • Jacob , V , Brasier , DJ , Erchova , I , Feldman , D and Shulz , DE . 2007 . “Spike timing‐dependent synaptic depression in the in vivo barrel cortex of the rat.” . J. Neurosci. , 27 : 1271 – 1284 .
  • Johnston , D , Christie , BR , Frick , A , Gray , R , Hoffman , DA , Schexnayder , LK , Watanabe , S and Yuan , LL . 2003 . “Active dendrites, potassium channels and synaptic plasticity.” . Philos. Trans. R. Soc. London, Ser. B , 358 : 667 – 674 .
  • Kampa , BM , Clements , J , Jonas , P and Stuart , GJ . 2004 . “Kinetics of Mg2+ unblock of NMDA receptors: implications for spike‐timing dependent synaptic plasticity.” . J. Physiol. , 556 : 337 – 345 .
  • Kampa , BM , Letzkus , JJ and Stuart , GJ . 2006 . “Requirement of dendritic calcium spikes for induction of spike‐timing‐dependent synaptic plasticity.” . J. Physiol. , 574 : 283 – 290 .
  • Kampa , BM , Letzkus , JJ and Stuart , GJ . 2007 . “Dendritic mechanisms controlling spike‐timing‐dependent synaptic plasticity.” . Trends Neurosci. , 30 : 456 – 463 .
  • Karmarkar , UR and Buonomano , DV . 2002 . “A model of spike‐timing dependent plasticity: one or two coincidence detectors?” . J. Neurophysiol. , 88 : 507 – 513 .
  • Koester , HJ and Sakmann , B . 1998 . “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.” . Proc. Natl. Acad. Sci. U.S.A. , 95 : 9596 – 9601 .
  • Krucker , T , Siggins , GR , McNamara , RK , Lindsley , KA , Dao , A , Allison , DW , de Lecea , L , Lovenberg , TW , Sutcliffe , JG and Gerendasy , DD . 2002 . “Targeted disruption of RC3 reveals a calmodulin‐based mechanism for regulating metaplasticity in the hippocampus.” . J. Neurosci. , 22 : 5525 – 5535 .
  • Krupp , JJ , Vissel , B , Thomas , CG , Heinemann , SF and Westbrook , GL . 1999 . “Interactions of calmodulin and alpha‐actinin with the NR1 subunit modulate Ca2+‐dependent inactivation of NMDA receptors.” . J. Neurosci. , 19 : 1165 – 1178 .
  • Kubota , S and Kitajima , T . 2008 . “A model for synaptic development regulated by NMDA receptor subunit expression.” . J. Comput. Neurosci. , 24 : 1 – 20 .
  • Kuroda , S , Schweighofer , N and Kawato , M . 2001 . “Exploration of signal transduction pathways in cerebellar long‐term depression by kinetic simulation.” . J. Neurosci. , 21 : 5693 – 5702 .
  • Larkum , ME and Nevian , T . 2008 . “Synaptic clustering by dendritic signaling mechanisms.” . Curr. Opin. Neurobiol. , 18 : 321 – 331 .
  • Lee , HK , Kameyama , K , Huganir , RL and Bear , MF . 1998 . “NMDA induces long‐term synaptic depression and dephosphorylation of the GluRl subunit of AMPA receptors in hippocampus.” . Neuron , 21 : 1151 – 1162 .
  • Lee , HK , Barbarosie , M , Kameyama , K , Bear , MF and Huganir , RL . 2000 . “Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity.” . Nature London , 405 : 955 – 959 .
  • Lee , SH , Liu , L , Wang , YT and Sheng , M . 2002 . “Clathrin adaptor AP2 and NSF interact with overlapping sites of GluR2 and play distinct roles in AMPA receptor trafficking and hippocampal LTD.” . Neuron , 36 : 661 – 674 .
  • Lee , SR , Escobedo‐Lozoya , Y , Szatmari , EM and Yasuda , R . 2009 . “Activation of CaMKII in single dendritic spines during long‐term potentiation.” . Nature London , 458 : 299 – 304 .
  • Letzkus , JJ , Kampa , BM and Stuart , GJ . 2006 . “Learning rules for spike timing‐dependent plasticity depend on dendritic synapse location.” . J. Neurosci , 26 : 10420 – 10429 .
  • Letzkus , JJ , Kampa , BM and Stuart , GJ . 2007 . “Does spike timing‐dependent synaptic plasticity underlie memory formation?” . Clin. Exp. Pharmacol. Physiol. , 34 : 1070 – 1076 .
  • Linden , DJ . 1999 . “The return of the spike: postsynaptic action potentials and the induction of LTP and LTD.” . Neuron , 22 : 661 – 666 .
  • Lisman , J , Schulman , H and Cline , H . 2002 . “The molecular basis of CaMKII function in synaptic and behavioural memory.” . Nat. Rev. Neurosci. , 3 : 175 – 190 .
  • Lisman , J and Spruston , N . 2005 . “Postsynaptic depolarization requirements for LTP and LTD: a critique of spike timing‐dependent plasticity.” . Nat. Neurosci. , 8 : 839 – 841 .
  • Lisman , JE . 2001 . “Three Ca2+ levels affect plasticity differently: the LTP zone, the LTD zone and no man's land.” . J. Physiol. , 532 : 285
  • Lisman , JE and Zhabotinsky , AM . 2001 . “A model of synaptic memory: a CaMKII/PP1 switch that potentiates transmission by organizing an AMPA receptor anchoring assembly.” . Neuron , 31 : 191 – 201 .
  • Luthi , A , Wikstrom , MA , Palmer , MJ , Matthews , P , Benke , TA , Isaac , JT and Collingridge , GL . 2004 . “Bi‐directional modulation of AMPA receptor unitary conductance by synaptic activity.” . BMC Neurosci. , 5 : 44
  • Magee , JC and Johnston , D . 1997 . “A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons.” . Science , 275 : 209 – 213 .
  • Malenka , RC and Bear , MF . 2004 . “LTP and LTD: an embarrassment of riches.” . Neuron , 44 : 5 – 21 .
  • Malinow , R , Schulman , H and Tsien , RW . 1989 . “Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP.” . Science , 245 : 862 – 866 .
  • Markram , H , Lubke , J , Frotscher , M and Sakmann , B . 1997 . “Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs.” . Science , 275 : 213 – 215 .
  • Matsuzaki , M , Honkura , N , Ellis‐Davies , GC and Kasai , H . 2004 . “Structural basis of long‐term potentiation in single dendritic spines.” . Nature London , 429 : 761 – 766 .
  • Meliza , CD and Dan , Y . 2006 . “Receptive‐field modification in rat visual cortex induced by paired visual stimulation and single‐cell spiking.” . Neuron , 49 : 183 – 189 .
  • Migliore , M , Hoffman , DA , Magee , JC and Johnston , D . 1999 . “Role of an A‐type K+ conductance in the back‐propagation of action potentials in the dendrites of hippocampal pyramidal neurons.” . J. Comput. Neurosci. , 7 : 5 – 15 .
  • Montgomery , JM and Madison , DV . 2002 . “State‐dependent heterogeneity in synaptic depression between pyramidal cell pairs.” . Neuron , 33 : 765 – 777 .
  • Morrison , A , Diesmann , M and Gerstner , W . 2008 . “Phenomenological models of synaptic plasticity based on spike timing.” . Biol. Cybern. , 98 : 459 – 478 .
  • Mu , Y and Poo , MM . 2006 . “Spike timing‐dependent LTP/LTD mediates visual experience‐dependent plasticity in a developing retinotectal system.” . Neuron , 50 : 115 – 125 .
  • Mulkey , RM , Herron , CE and Malenka , RC . 1993 . “An essential role for protein phosphatases in hippocampal long‐term depression.” . Science , 261 : 1051 – 1055 .
  • Nagerl , UV , Eberhorn , N , Cambridge , SB and Bonhoeffer , T . 2004 . “Bidirectional activity‐dependent morphological plasticity in hippocampal neurons.” . Neuron , 44 : 759 – 767 .
  • Nevian , T and Sakmann , B . 2004 . “Single spine Ca2+ signals evoked by coincident EPSPs and backpropagating action potentials in spiny stellate cells of layer 4 in the juvenile rat somatosensory barrel cortex.” . J. Neurosci. , 24 : 1689 – 1699 .
  • Nevian , T and Sakmann , B . 2006 . “Spine Ca2+ signaling in spike‐timing‐dependent plasticity.” . J. Neurosci. , 26 : 11001 – 11013 .
  • Nishiyama , M , Hong , K , Mikoshiba , K , Poo , MM and Kato , K . 2000 . “Calcium stores regulate the polarity and input specificity of synaptic modification.” . Nature London , 408 : 584 – 588 .
  • Normann , C , Peckys , D , Schulze , CH , Waiden , J , Jonas , P and Bischofberger , J . 2000 . “Associative long‐term depression in the hippocampus is dependent on postsynaptic N‐type Ca2+channels.” . J. Neurosci. , 20 : 8290 – 8297 .
  • O'Connor , DH , Wittenberg , GM and Wang , SS . 2005 . “Graded bidirectional synaptic plasticity is composed of switch‐like unitary events.” . Proc. Natl. Acad. Sci. U.S.A. , 102 : 9679 – 9684 .
  • Okamoto , H and Ichikawa , K . 2000 . “Switching characteristics of a model for biochemical‐reaction networks describing autophosphorylation versus dephosphorylation of Ca2+/calmodulin‐dependent protein kinase II.” . Biol. Cybern. , 82 : 35 – 47 .
  • Okamoto , K , Nagai , T , Miyawaki , A and Hayashi , Y . 2004 . “Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity.” . Nat. Neurosci. , 7 : 1104 – 1112 .
  • Okamoto , K , Narayanan , R , Lee , SH , Murata , K and Hayashi , Y . 2007 . “The role of CaMKII as an F‐actin‐bundling protein crucial for maintenance of dendritic spine structure.” . Proc. Natl. Acad. Sci. U.S.A. , 104 : 6418 – 6423 .
  • Otmakhov , N , Griffith , LC and Lisman , JE . 1997 . “Postsynaptic inhibitors of calcium/calmodulin‐dependent protein kinase type II block induction but not maintenance of pairing‐induced long‐term potentiation.” . J. Neurosci. , 17 : 5357 – 5365 .
  • Pawlak , V and Kerr , JN . 2008 . “Dopamine receptor activation is required for corticostriatal spike‐timing‐dependent plasticity.” . J. Neurosci. , 28 : 2435 – 2446 .
  • Petersen , CC , Malenka , RC , Nicoll , RA and Hopfield , JJ . 1998 . “All‐or‐none potentiation at CA3‐CA1 synapses.” . Proc. Natl. Acad. Sci. U.S.A. , 95 : 4732 – 4737 .
  • Pfister , JP and Gerstner , W . 2006 . “Triplets of spikes in a model of spike timing‐dependent plasticity.” . J. Neurosci. , 26 : 9673 – 9682 .
  • Pi , HJ and Lisman , JE . 2008 . “Coupled phosphatase and kinase switches produce the tristability required for long‐term potentiation and long‐term depression.” . J. Neurosci. , 28 : 13132 – 13138 .
  • Pike , FG , Meredith , RM , Olding , AW and Paulsen , O . 1999 . “Rapid report: postsynaptic bursting is essential for ‘Hebbian’ induction of associative long‐term potentiation at excitatory synapses in rat hippocampus.” . J. Physiol. , 518 (Pt 2) : 571 – 576 .
  • Poirazi , P , Brannon , T and Mel , BW . 2003 . “Arithmetic of subthreshold synaptic summation in a model CA1 pyramidal cell.” . Neuron , 37 : 977 – 987 .
  • Rodriguez‐Moreno , A and Paulsen , O . 2008 . “Spike timing‐dependent long‐term depression requires presynaptic NMDA receptors.” . Nat. Neurosci. , 11 : 744 – 745 .
  • Rose , J , Jin , SX and Craig , AM . 2009 . “Heterosynaptic molecular dynamics: locally induced propagating synaptic accumulation of CaM kinase II.” . Neuron , 61 : 351 – 358 .
  • Rubin , JE , Gerkin , RC , Bi , GQ and Chow , CC . 2005 . “Calcium time course as a signal for spike‐timing‐dependent plasticity.” . J. Neurophysiol. , 93 : 2600 – 2613 .
  • Rycroft , BK and Gibb , AJ . 2002 . “Direct effects of calmodulin on NMDA receptor single‐channel gating in rat hippocampal granule cells.” . J. Neurosci. , 22 : 8860 – 8868 .
  • Rycroft , BK and Gibb , AJ . 2004 . “Inhibitory interactions of calcineurin (phosphatase 2B) and calmodulin on rat hippocampal NMDA receptors.” . Neuropharmacology , 47 : 505 – 514 .
  • Sanhueza , M , McIntyre , CC and Lisman , JE . 2007 . “Reversal of synaptic memory by Ca2+/calmodulin‐dependent protein kinase II inhibitor.” . J. Neurosci. , 27 : 5190 – 5199 .
  • Schaefer , AT , Larkum , ME , Sakmann , B and Roth , A . 2003 . “Coincidence detection in pyramidal neurons is tuned by their dendritic branching pattern.” . J. Neurophysiol. , 89 : 3143 – 3154 .
  • Schiller , J , Schiller , Y and Clapham , DE . 1998 . “NMDA receptors amplify calcium influx into dendritic spines during associative pre‐ and postsynaptic activation.” . Nat. Neurosci. , 1 : 114 – 118 .
  • Schlieft , S , Bonhoeffer , T and Hubener , M . 2001 . “Pairing‐induced changes of orientation maps in cat visual cortex.” . Neuron , 32 : 325 – 337 .
  • Seol , GH , Ziburkus , J , Huang , S , Song , L , Kim , IT , Takamiya , K , Huganir , RL , Lee , HK and Kirkwood , A . 2007 . “Neuromodulators control the polarity of spike‐timing‐dependent synaptic plasticity.” . Neuron , 55 : 919 – 929 .
  • Shouval , HZ . 2005 . “Clusters of interacting receptors can stabilize synaptic efficacies.” . Proc. Natl. Acad. Sci. U.S.A. , 102 : 14440 – 14445 .
  • Shouval , HZ , Bear , MF and Cooper , LN . 2002 . “A unified model of NMDA receptor‐dependent bidirectional synaptic plasticity.” . Proc. Natl. Acad. Sci. U.S.A. , 99 : 10831 – 10836 .
  • Sjostrom , PJ and Hausser , M . 2006 . “A cooperative switch determines the sign of synaptic plasticity in distal dendrites of neocortical pyramidal neurons.” . Neuron , 51 : 227 – 238 .
  • Sjostrom , PJ and Nelson , SB . 2002 . “Spike timing, calcium signals and synaptic plasticity.” . Curr. Opin. Neurobiol. , 12 : 305 – 314 .
  • Sjostrom , PJ , Rancz , EA , Roth , A and Hausser , M . 2008 . “Dendritic excitability and synaptic plasticity.” . Physiol. Rev. , 88 : 769 – 840 .
  • Sjostrom , PJ , Turrigiano , GG and Nelson , SB . 2001 . “Rate, timing, and cooperativity jointly determine cortical synaptic plasticity.” . Neuron , 32 : 1149 – 1164 .
  • Sjostrom , PJ , Turrigiano , GG and Nelson , SB . 2003 . “Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors.” . Neuron , 39 : 641 – 654 .
  • Sjostrom , PJ , Turrigiano , GG and Nelson , SB . 2004 . “Endocannabinoid‐dependent neocortical layer‐5 LTD in the absence of postsynaptic spiking.” . J. Neurophysiol. , 92 : 3338 – 3343 .
  • Softky , WR and Koch , C . 1993 . “The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs.” . J. Neurosci. , 13 : 334 – 350 .
  • Song , S , Miller , KD and Abbott , LF . 2000 . “Competitive Hebbian learning through spike‐timing‐dependent synaptic plasticity.” . Nat. Neurosci. , 3 : 919 – 926 .
  • Spruston , N . 2008 . “Pyramidal neurons: dendritic structure and synaptic integration.” . Nat. Rev. Neurosci. , 9 : 206 – 221 .
  • Spruston , N , Schiller , Y , Stuart , G and Sakmann , B . 1995 . “Activity‐dependent action potential invasion and calcium influx into hippocampal CA1 dendrites.” . Science , 268 : 297 – 300 .
  • Staubli , U and Chun , D . 1996 . “Factors regulating the reversibility of long‐term potentiation.” . J. Neurosci. , 16 : 853 – 860 .
  • Steriade , M . 2004 . “Neocortical cell classes are flexible entities.” . Nat. Rev. Neurosci. , 5 : 121 – 134 .
  • Stuart , GJ and Hausser , M . 2001 . “Dendritic coincidence detection of EPSPs and action potentials.” . Nat. Neurosci. , 4 : 63 – 71 .
  • Tong , G , Shepherd , D and Jahr , CE . 1995 . “Synaptic desensitization of NMDA receptors by calcineurin.” . Science , 267 : 1510 – 1512 .
  • Tzounopoulos , T , Kim , Y , Oertel , D and Trussell , LO . 2004 . “Cell‐specific, spike timing‐dependent plasticities in the dorsal cochlear nucleus.” . Nat. Neurosci. , 7 : 719 – 725 .
  • Tzounopoulos , T , Rubio , ME , Keen , JE and Trussell , LO . 2007 . “Coactivation of pre‐ and postsynaptic signaling mechanisms determines cell‐specific spike‐timing‐dependent plasticity.” . Neuron , 54 : 291 – 301 .
  • Umemiya , M , Chen , N , Raymond , LA and Murphy , TH . 2001 . “A calcium‐dependent feedback mechanism participates in shaping single NMDA miniature EPSCs.” . J. Neurosci. , 21 : 1 – 9 .
  • Urakubo , H , Aihara , T , Kuroda , S , Watanabe , M and Kondo , S . 2004 . “Spatial localization of synapses required for supralinear summation of action potentials and EPSPs.” . J. Comput. Neurosci. , 16 : 251 – 256 .
  • Urakubo , H , Honda , M , Froemke , RC and Kuroda , S . 2008 . “Requirement of an allosteric kinetics of NMDA receptors for spike timing‐dependent plasticity.” . J. Neurosci. , 28 : 3310 – 3323 .
  • van Rossum , MC , Bi , GQ and Turrigiano , GG . 2000 . “Stable Hebbian learning from spike timing‐dependent plasticity.” . J. Neurosci. , 20 : 8812 – 8821 .
  • Vislay‐Meltzer , RL , Kampff , AR and Engert , F . 2006 . “Spatiotemporal specificity of neuronal activity directs the modification of receptive fields in the developing retinotectal system.” . Neuron , 50 : 101 – 114 .
  • Wang , HX , Gerkin , RC , Nauen , DW and Bi , GQ . 2005 . “Coactivation and timing‐dependent integration of synaptic potentiation and depression.” . Nat. Neurosci. , 8 : 187 – 193 .
  • Wang , XB , Yang , Y and Zhou , Q . 2007 . “Independent expression of synaptic and morphological plasticity associated with long‐term depression.” . J. Neurosci. , 27 : 12419 – 12429 .
  • Watanabe , S , Hoffman , DA , Migliore , M and Johnston , D . 2002 . “Dendritic K+ channels contribute to spike‐timing dependent long‐term potentiation in hippocampal pyramidal neurons.” . Proc. Natl. Acad. Sci. U.S.A. , 99 : 8366 – 8371 .
  • Waters , J and Helmchen , F . 2004 . “Boosting of action potential backpropagation by neocortical network activity in vivo.” . J. Neurosci. , 24 : 11127 – 11136 .
  • Wittenberg , GM and Wang , SS . 2006 . “Malleability of spike‐timing‐dependent plasticity at the CA3‐CA1 synapse.” . J. Neurosci. , 26 : 6610 – 6617 .
  • Wolters , A , Sandbrink , F , Schlottmann , A , Kunesch , E , Stefan , K , Cohen , LG , Benecke , R and Classen , J . 2003 . “A temporally asymmetric Hebbian rule governing plasticity in the human motor cortex.” . J. Neurophysiol. , 89 : 2339 – 2345 .
  • Worgotter , F and Porr , B . 2005 . “Temporal sequence learning, prediction and control: a review of different models and their relation to biological mechanisms.” . Neural Comput. , 17 : 245 – 319 .
  • Yang , Y , Wang , XB , Frerking , M and Zhou , Q . 2008 . “Spine expansion and stabilization associated with long‐term potentiation.” . J. Neurosci. , 28 : 5740 – 5751 .
  • Yao , H and Dan , Y . 2001 . “Stimulus timing‐dependent plasticity in cortical processing of orientation.” . Neuron , 32 : 315 – 323 .
  • Yao , H , Shen , Y and Dan , Y . 2004 . “Intracortical mechanism of stimulus‐timing‐dependent plasticity in visual cortical orientation tuning.” . Proc. Natl. Acad. Sci. U.S.A. , 101 : 5081 – 5086 .
  • Zhabotinsky , AM . 2000 . “Bistability in the Ca2+/calmodulin‐dependent protein kinase‐phosphatase system.” . Biophys. J. , 79 : 2211 – 2221 .
  • Zhang , LI , Tao , HW , Holt , CE , Harris , WA and Poo , M . 1998a . “A critical window for cooperation and competition among developing retinotectal synapses.” . Nature London , 395 : 37 – 44 .
  • Zhang , S , Ehlers , MD , Bernhardt , JP , Su , CT and Huganir , RL . 1998b . “Calmodulin mediates calcium‐dependent inactivation of N‐methyl‐D‐aspartate receptors.” . Neuron , 21 : 443 – 453 .
  • Zhou , Q , Homma , KJ and Poo , MM . 2004 . “Shrinkage of dendritic spines associated with long‐term depression of hippocampal synapses.” . Neuron , 44 : 749 – 757 .
  • Zhou , Q , Tao , HW and Poo , MM . 2003 . “Reversal and stabilization of synaptic modifications in a developing visual system.” . Science , 300 : 1953 – 1957 .
  • Zhuo , M , Zhang , W , Son , H , Mansuy , I , Sobel , RA , Seidman , J and Kandel , ER . 1999 . “A selective role of calcineurin Aα in synaptic depotentiation in hippocampus.” . Proc. Natl. Acad. Sci. U.S.A. , 96 : 4650 – 4655 .
  • Zucker , RS . 1999 . “Calcium‐ and activity‐dependent synaptic plasticity.” . Curr. Opin. Neurobiol. , 9 : 305 – 313 .

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