LTP and LTD

Neuron - Tập 44 - Trang 5-21 - 2004
Robert C. Malenka1, Mark F. Bear2
1Nancy Pritzker Laboratory, Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Palo Alto, CA 94304 USA
2Howard Hughes Medical Institute and the, Picower Center for Learning and Memory, Massachusetts Institute of Technology, Cambridge, MA 02139 USA

Tài liệu tham khảo

Abraham, 1996, Metaplasticity, Trends Neurosci, 19, 126, 10.1016/S0166-2236(96)80018-X Abraham, 2003, Properties and mechanisms of LTP maintenance, Neuroscientist, 9, 463, 10.1177/1073858403259119 Aiba, 1994, Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice, Cell, 79, 377, 10.1016/0092-8674(94)90205-4 Allen, 2003, Long-term depression induced by sensory deprivation during cortical map plasticity in vivo, Nat. Neurosci, 6, 291, 10.1038/nn1012 Banke, 2000, Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase, J. Neurosci, 20, 89, 10.1523/JNEUROSCI.20-01-00089.2000 Barria, 2002, Subunit-specific NMDA receptor trafficking to synapses, Neuron, 35, 345, 10.1016/S0896-6273(02)00776-6 Barria, 1997, Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation, Science, 276, 2042, 10.1126/science.276.5321.2042 Barrionuevo, 1980, The effects of repetitive low frequency stimulation on control and “potentiated” synaptic responses in the hippocampus, Life Sci, 27, 2385, 10.1016/0024-3205(80)90509-3 Bear, 2003, Bidirectional synaptic plasticity, Philos. Trans. R. Soc. Lond. B Biol. Sci, 358, 649, 10.1098/rstb.2002.1255 Bear, 1994, Synaptic plasticity, Curr. Opin. Neurobiol, 4, 389, 10.1016/0959-4388(94)90101-5 Bear, 1990, Disruption of experience-dependent synaptic modifications in striate cortex by infusion of an NMDA receptor antagonist, J. Neurosci, 10, 909, 10.1523/JNEUROSCI.10-03-00909.1990 Beattie, 2000, Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD, Nat. Neurosci, 3, 1291, 10.1038/81823 Benke, 1998, Modulation of AMPA receptor unitary conductance by synaptic activity, Nature, 393, 793, 10.1038/31709 Berke, 2000, Addiction, dopamine, and the molecular mechanisms of memory, Neuron, 25, 515, 10.1016/S0896-6273(00)81056-9 Bhalla, 1999, Emergent properties of networks of biological signaling pathways, Science, 283, 381, 10.1126/science.283.5400.381 Bienenstock, 1982, Theory for the development of neuron selectivity, J. Neurosci, 2, 32, 10.1523/JNEUROSCI.02-01-00032.1982 Bliss, 1993, A synaptic model of memory, Nature, 361, 31, 10.1038/361031a0 Blitzer, 1998, Gating of CaMKII by cAMP-regulated protein phosphatase activity during LTP, Science, 280, 1940, 10.1126/science.280.5371.1940 Bolshakov, 1994, Postsynaptic induction and presynaptic expression of hippocampal long-term depression, Science, 264, 1148, 10.1126/science.7909958 Bolshakov, 2000, Dual MAP kinase pathways mediate opposing forms of long-term plasticity at CA3–CA1 synapses, Nat. Neurosci, 3, 1107, 10.1038/80624 Borgland, 2004, Acute and chronic cocaine-induced potentiation of synaptic strength in the ventral tegmental area, J. Neurosci, 24, 7482, 10.1523/JNEUROSCI.1312-04.2004 Bredt, 2003, AMPA receptor trafficking at excitatory synapses, Neuron, 40, 361, 10.1016/S0896-6273(03)00640-8 Brown, 2000, Long-term potentiation induced by theta frequency stimulation is regulated by a protein phosphatase-1-operated gate, J. Neurosci, 20, 7880, 10.1523/JNEUROSCI.20-21-07880.2000 Burbea, 2002, Ubiquitin and AP180 regulate the abundance of GLR-1 glutamate receptors at postsynaptic elements in C. elegans, Neuron, 35, 107, 10.1016/S0896-6273(02)00749-3 Calixto, 2003, Early maintenance of hippocampal mossy fiber–long-term potentiation depends on protein and RNA synthesis and presynaptic granule cell integrity, J. Neurosci, 23, 4842, 10.1523/JNEUROSCI.23-12-04842.2003 Carlezon, 2002, Elevated levels of GluR1 in the midbrain, Trends Neurosci, 25, 610, 10.1016/S0166-2236(02)02289-0 Carlezon, 1997, Sensitization to morphine induced by viral-mediated gene transfer, Science, 277, 812, 10.1126/science.277.5327.812 Carroll, 1999, Rapid redistribution of glutamate receptors contributes to long-term depression in hippocampal cultures, Nat. Neurosci, 2, 454, 10.1038/8123 Carroll, 2001, Role of AMPA receptor endocytosis in synaptic plasticity, Nat. Rev. Neurosci, 2, 315, 10.1038/35072500 Castillo, 1994, The role of Ca2+ channels in hippocampal mossy fiber synaptic transmission and long-term potentiation, Neuron, 12, 261, 10.1016/0896-6273(94)90269-0 Castillo, 1997, Rab3A is essential for mossy fibre long-term potentiation in the hippocampus, Nature, 388, 590, 10.1038/41574 Castillo, 2002, RIM1alpha is required for presynaptic long-term potentiation, Nature, 415, 327, 10.1038/415327a Castro-Alamancos, 1999, Presynaptic long-term potentiation in corticothalamic synapses, J. Neuroscience, 19, 9090, 10.1523/JNEUROSCI.19-20-09090.1999 Celikel, 2004, Modulation of spike timing by sensory deprivation during induction of cortical map plasticity, Nat. Neurosci, 7, 534, 10.1038/nn1222 Chen, 2000, Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms, Nature, 408, 936, 10.1038/35046031 Chevaleyre, 2002, Assessing the role of Ih channels in synaptic transmission and mossy fiber LTP, Proc. Natl. Acad. Sci. USA, 99, 9538, 10.1073/pnas.142213199 Chevaleyre, 2003, Heterosynaptic LTD of hippocampal GABAergic synapses, Neuron, 38, 461, 10.1016/S0896-6273(03)00235-6 Choi, 2000, Postfusional regulation of cleft glutamate concentration during LTP at 'silent synapses', Nat. Neuroscience, 3, 330, 10.1038/73895 Choi, 2003, Opposite effects of GluR1 and PKA-resistant GluR1 overexpression in the ventral tegmental area on cocaine reinforcement, Ann. N Y Acad. Sci, 1003, 372, 10.1196/annals.1300.029 Chung, 2003, Requirement of AMPA receptor GluR2 phosphorylation for cerebellar long-term depression, Science, 300, 1751, 10.1126/science.1082915 Cline, 2003, Synaptic plasticity, Curr. Biol, 13, R514, 10.1016/S0960-9822(03)00443-3 Colledge, 2003, Ubiquitination regulates PSD-95 degradation and AMPA receptor surface expression, Neuron, 40, 595, 10.1016/S0896-6273(03)00687-1 Contractor, 2001, Kainate receptors are involved in short- and long-term plasticity at mossy fiber synapses in the hippocampus, Neuron, 29, 209, 10.1016/S0896-6273(01)00191-X Contractor, 2002, Trans-synaptic Eph receptor-ephrin signaling in hippocampal mossy fiber LTP, Science, 296, 1864, 10.1126/science.1069081 Cummings, 1996, Ca2+ signaling requirements for long-term depression in the hippocampus, Neuron, 16, 825, 10.1016/S0896-6273(00)80102-6 Daw, 2000, PDZ proteins interacting with C-terminal GluR2/3 are involved in a PKC-dependent regulation of AMPA receptors at hippocampal synapses, Neuron, 28, 873, 10.1016/S0896-6273(00)00160-4 Daw, 2002, Phosphatidylinositol 3 kinase regulates synapse specificity of hippocampal long-term depression, Nat. Neurosci, 5, 835, 10.1038/nn903 Dodt, 1999, Precisely localized LTD in the neocortex revealed by infrared-guided laser stimulation, Science, 286, 110, 10.1126/science.286.5437.110 Doherty, 2000, A novel, competitive mGlu(5) receptor antagonist (LY344545) blocks DHPG-induced potentiation of NMDA responses but not the induction of LTP in rat hippocampal slices, Br. J. Pharmacol, 131, 239, 10.1038/sj.bjp.0703574 Dong, 2004, Cocaine-induced potentiation of synaptic strength in dopamine neurons, Proc. Natl. Acad. Sci. USA, 101, 14282, 10.1073/pnas.0401553101 Dudek, 1992, Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade, Proc. Natl. Acad. Sci. USA, 89, 4363, 10.1073/pnas.89.10.4363 Dudek, 1993, Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus, J. Neurosci, 13, 2910, 10.1523/JNEUROSCI.13-07-02910.1993 Ehlers, 2000, Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting, Neuron, 28, 511, 10.1016/S0896-6273(00)00129-X Ehlers, 2003, Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system, Nat. Neurosci, 6, 231, 10.1038/nn1013 El-Husseini Ael, 2002, Synaptic strength regulated by palmitate cycling on PSD-95, Cell, 108, 849, 10.1016/S0092-8674(02)00683-9 Emptage, 2003, Optical quantal analysis reveals a presynaptic component of LTP at hippocampal Schaffer-associational synapses, Neuron, 38, 797, 10.1016/S0896-6273(03)00325-8 Endo, 2003, ERKs regulate PKC-dependent synaptic depression and declustering of glutamate receptors in cerebellar Purkinje cells, Neuropharmacology, 45, 863, 10.1016/S0028-3908(03)00210-7 Esteban, 2003, PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity, Nat. Neurosci, 6, 136, 10.1038/nn997 Everitt, 2002, Psychomotor stimulant addiction, J. Neurosci, 22, 3312, 10.1523/JNEUROSCI.22-09-03312.2002 Faas, 2002, Modulation of presynaptic calcium transients by metabotropic glutamate receptor activation, J. Neurosci, 22, 6885, 10.1523/JNEUROSCI.22-16-06885.2002 Faleiro, L.J., Jones, S., and Kauer, J.A. (2004). Rapid synaptic plasticity of glutamatergic synapses on dopamine neurons in the ventral tegmental area in response to acute amphetamine injection. Neuropsychopharmacology, in press. Published online May 19, 2004. 10.1038/sj.npp.1300495. Feinmark, 2003, 12-lipoxygenase metabolites of arachidonic acid mediate metabotropic glutamate receptor-dependent long-term depression at hippocampal CA3–CA1 synapses, J. Neurosci, 23, 11427, 10.1523/JNEUROSCI.23-36-11427.2003 Feldman, 2000, Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex, Neuron, 27, 45, 10.1016/S0896-6273(00)00008-8 Fitzjohn, 2001, A characterisation of long-term depression induced by metabotropic glutamate receptor activation in the rat hippocampus in vitro, J. Physiol, 537, 421, 10.1111/j.1469-7793.2001.00421.x Freund, 2003, Role of endogenous cannabinoids in synaptic signaling, Physiol. Rev, 83, 1017, 10.1152/physrev.00004.2003 Frey, 1998, Synaptic tagging, Trends Neurosci, 21, 181, 10.1016/S0166-2236(97)01189-2 Fujii, 1991, Reversal of long-term potentiation (depotentiation) induced by tetanus stimulation of the input to CA1 neurons of guinea pig hippocampal slices, Brain Res, 555, 112, 10.1016/0006-8993(91)90867-U Fukazawa, 2003, Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo, Neuron, 38, 447, 10.1016/S0896-6273(03)00206-X Gallagher, 2004, Extracellular signal-regulated protein kinase activation is required for metabotropic glutamate receptor-dependent long-term depression in hippocampal area CA1, J. Neurosci, 24, 4859, 10.1523/JNEUROSCI.5407-03.2004 Gean, 1993, D-2-amino-5-phosphonovaleate blocks induction of long-term depression of the NMDA receptor-mediated synaptic component in rat hippocampus, Neurosci. Lett, 158, 170, 10.1016/0304-3940(93)90256-K Gerdeman, 2002, Postsynaptic endocannabinoid release is critical to long-term depression in the striatum, Nat. Neurosci, 5, 446, 10.1038/nn832 Gerdeman, 2003, It could be habit forming, Trends Neurosci, 26, 184, 10.1016/S0166-2236(03)00065-1 Gomez, 2002, Regulation of A-kinase anchoring protein 79/150-cAMP-dependent protein kinase postsynaptic targeting by NMDA receptor activation of calcineurin and remodeling of dendritic actin, J. Neurosci, 22, 7027, 10.1523/JNEUROSCI.22-16-07027.2002 Gutlerner, 2002, Novel protein kinase A-dependent long-term depression of excitatory synapses, Neuron, 36, 921, 10.1016/S0896-6273(02)01051-6 Harris, 2003, Critical role for ventral tegmental glutamate in preference for a cocaine-conditioned environment, Neuropsychopharmacology, 28, 73, 10.1038/sj.npp.1300011 Harris, 1986, Long-term potentiation of guinea pig mossy fiber responses is not blocked by N-methyl D-aspartate antagonists, Neurosci. Lett, 70, 132, 10.1016/0304-3940(86)90451-9 Hayashi, 2000, Driving AMPA receptors into synapses by LTP and CaMKII, Science, 287, 2262, 10.1126/science.287.5461.2262 Hegde, 2002, Ubiquitin and the synapse, Nat. Rev. Neurosci, 3, 854, 10.1038/nrn961 Hendricson, 2002, Ifenprodil and ethanol enhance NMDA receptor-dependent long-term depression, J. Pharmacol. Exp. Ther, 301, 938, 10.1124/jpet.301.3.938 Henze, 2000, The multifarious hippocampal mossy fiber pathway, Neuroscience, 98, 407, 10.1016/S0306-4522(00)00146-9 Hering, 2001, Dendritic spines, Nat. Rev. Neurosci, 2, 880, 10.1038/35104061 Heynen, 2000, Bidirectional, activity-dependent regulation of glutamate receptors in the adult hippocampus in vivo, Neuron, 28, 527, 10.1016/S0896-6273(00)00130-6 Heynen, 2003, Molecular mechanism for loss of visual cortical responsiveness following brief monocular deprivation, Nat. Neurosci, 6, 854, 10.1038/nn1100 Hoffman, 2002, Molecular dissection of hippocampal theta-burst pairing potentiation, Proc. Natl. Acad. Sci. USA, 99, 7740, 10.1073/pnas.092157999 Hoffman, 2003, Functional tolerance and blockade of long-term depression at synapses in the nucleus accumbens after chronic cannabinoid exposure, J. Neurosci, 23, 4815, 10.1523/JNEUROSCI.23-12-04815.2003 Hou, 2004, Activation of the phosphoinositide 3-kinase-Akt-mammalian target of rapamycin signaling pathway is required for metabotropic glutamate receptor-dependent long-term depression, J. Neurosci, 24, 6352, 10.1523/JNEUROSCI.0995-04.2004 Hrabetova, 1996, Bidirectional regulation of protein kinase M zeta in the maintenance of long-term potentiation and long-term depression, J. Neurosci, 16, 5324, 10.1523/JNEUROSCI.16-17-05324.1996 Hrabetova, 2001, Transient translocation of conventional protein kinase C isoforms and persistent downregulation of atypical protein kinase Mzeta in long-term depression, Brain Res. Mol. Brain Res, 95, 146, 10.1016/S0169-328X(01)00185-1 Hrabetova, 2000, Distinct NMDA receptor subpopulations contribute to long-term potentiation and long-term depression induction, J. Neurosci, 20, RC81, 10.1523/JNEUROSCI.20-12-j0002.2000 Hu, 1987, Protein kinase C injection into hippocampal pyramidal cells elicits features of long term potentiation, Nature, 328, 426, 10.1038/328426a0 Huang, 1994, cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase, Cell, 79, 69, 10.1016/0092-8674(94)90401-4 Huber, 2000, Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression, Science, 288, 1254, 10.1126/science.288.5469.1254 Huber, 2001, Chemical induction of mGluR5- and protein synthesis–dependent long-term depression in hippocampal area CA1, J. Neurophysiol, 86, 321, 10.1152/jn.2001.86.1.321 Hyman, 2001, Addiction and the brain, Nat. Rev. Neurosci, 2, 695, 10.1038/35094560 Ito, 1989, Long term depression, Ann. Rev. Neurosci, 12, 85, 10.1146/annurev.ne.12.030189.000505 Ito, 1982, Climbing fibre induced depression of both mossy fibre responsiveness and glutamate sensitivity of cerebellar Purkinje cells, J. Physiol, 324, 113, 10.1113/jphysiol.1982.sp014103 Jensen, 2003, A juvenile form of postsynaptic hippocampal long-term potentiation in mice deficient for the AMPA receptor subunit GluR-A, J. Physiol, 553, 843, 10.1113/jphysiol.2003.053637 Jia, 1996, Enhanced LTP in mice deficient in the AMPA receptor GluR2, Neuron, 17, 945, 10.1016/S0896-6273(00)80225-1 Jones, 2000, Amphetamine blocks long-term synaptic depression in the ventral tegmental area, J. Neurosci, 20, 5575, 10.1523/JNEUROSCI.20-15-05575.2000 Ju, 2004, Activity-dependent regulation of dendritic synthesis and trafficking of AMPA receptors, Nat. Neurosci, 7, 244, 10.1038/nn1189 Kamal, 1999, Chemical LTD in the CA1 field of the hippocampus from young and mature rats, Eur. J. Neurosci, 11, 3512, 10.1046/j.1460-9568.1999.00769.x Kameyama, 1998, Involvement of a postsynaptic protein kinase A substrate in the expression of homosynaptic long-term depression, Neuron, 21, 1163, 10.1016/S0896-6273(00)80633-9 Kamiya, 2002, Presynaptic Ca2+ entry is unchanged during hippocampal mossy fiber long-term potentiation, J. Neurosci, 22, 10524, 10.1523/JNEUROSCI.22-24-10524.2002 Kandler, 1998, Focal photolysis of caged glutamate produces long-term depression of hippocampal glutamate receptors, Nat. Neurosci, 1, 119, 10.1038/368 Karachot, 2001, Induction of long-term depression in cerebellar Purkinje cells requires a rapidly turned over protein, J. Neurophysiol, 86, 280, 10.1152/jn.2001.86.1.280 Kauderer, 2000, Capture of a protein synthesis-dependent component of long-term depression, Proc. Natl. Acad. Sci. USA, 97, 13342, 10.1073/pnas.97.24.13342 Kauer, 2004, Learning mechanisms in addiction, Annu. Rev. Physiol, 66, 447, 10.1146/annurev.physiol.66.032102.112534 Kauer, 1988, NMDA application potentiates synaptic transmission in the hippocampus, Nature, 334, 250, 10.1038/334250a0 Kawamura, 2004, Glutamate release increases during mossy-CA3 LTP but not during Schaffer-CA1 LTP, Eur. J. Neurosci, 19, 1591, 10.1111/j.1460-9568.2004.03258.x Kelley, 2004, Memory and addiction, Neuron, 44, 161, 10.1016/j.neuron.2004.09.016 Kelley, 2002, The neuroscience of natural rewards, J. Neurosci, 22, 3306, 10.1523/JNEUROSCI.22-09-03306.2002 Kelz, 1999, Expression of the transcription factor deltaFosB in the brain controls sensitivity to cocaine, Nature, 401, 272, 10.1038/45790 Kemp, 1997, NMDA receptor-dependent and -independent long-term depression in the CA1 region of the adult rat hippocampus in vitro, Neuropharmacology, 36, 397, 10.1016/S0028-3908(96)90015-5 Kemp, 2000, Different forms of LTD in the CA1 region of the hippocampus, Eur. J. Neurosci, 12, 360, 10.1046/j.1460-9568.2000.00903.x Kim, 1999, A role of actin filament in synaptic transmission and long-term potentiation, J. Neurosci, 19, 4314, 10.1523/JNEUROSCI.19-11-04314.1999 Kim, 2001, Interaction of the AMPA receptor subunit GluR2/3 with PDZ domains regulates hippocampal long-term depression, Proc. Natl. Acad. Sci. USA, 98, 11725, 10.1073/pnas.211132798 Kirkwood, 1994, Homosynaptic long-term depression in the visual cortex, J. Neurosci, 14, 3404, 10.1523/JNEUROSCI.14-05-03404.1994 Kirkwood, 1993, Common forms of synaptic plasticity in the hippocampus and neocortex in vitro, Science, 260, 1518, 10.1126/science.8502997 Kirkwood, 1999, Modulation of long-term synaptic depression in visual cortex by acetylcholine and norepinephrine, J. Neurosci, 19, 1599, 10.1523/JNEUROSCI.19-05-01599.1999 Kirkwood, 1997, Age-dependent decrease of synaptic plasticity in the neocortex of alphaCaMKII mutant mice, Proc. Natl. Acad. Sci. USA, 94, 3380, 10.1073/pnas.94.7.3380 Kreitzer, 2001, Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells, Neuron, 29, 717, 10.1016/S0896-6273(01)00246-X Kreitzer, 2002, Retrograde signaling by endocannabinoids, Curr. Opin. Neurobiol, 12, 324, 10.1016/S0959-4388(02)00328-8 Krucker, 2000, Dynamic actin filaments are required for stable long-term potentiation (LTP) in area CA1 of the hippocampus, Proc. Natl. Acad. Sci. USA, 97, 6856, 10.1073/pnas.100139797 Kullmann, 1995, The site of expression of NMDA receptor-dependent LTP, Neuron, 15, 997, 10.1016/0896-6273(95)90089-6 Lai, 1999, The calcineurin-dynamin 1 complex as a calcium sensor for synaptic vesicle endocytosis, J. Biol. Chem, 274, 25963, 10.1074/jbc.274.37.25963 Lauri, 2001, A critical role of a facilitatory presynaptic kainate receptor in mossy fiber LTP, Neuron, 32, 697, 10.1016/S0896-6273(01)00511-6 Lauri, 2003, A role for Ca2+ stores in kainate receptor-dependent synaptic facilitation and LTP at mossy fiber synapses in the hippocampus, Neuron, 39, 327, 10.1016/S0896-6273(03)00369-6 Lee, 1998, NMDA induces long-term synaptic depression and dephosphorylation of the GluR1 subunit of AMPA receptors in hippocampus, Neuron, 21, 1151, 10.1016/S0896-6273(00)80632-7 Lee, 2000, Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity, Nature, 405, 955, 10.1038/35016089 Lee, 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, 10.1016/S0896-6273(02)01024-3 Lee, 2003, Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory, Cell, 112, 631, 10.1016/S0092-8674(03)00122-3 Leonard, 1999, Calcium/calmodulin-dependent protein kinase II is associated with the N-methyl-D-aspartate receptor, Proc. Natl. Acad. Sci. USA, 96, 3239, 10.1073/pnas.96.6.3239 Li, 2001, Induction of mossy fiber → Ca3 long-term potentiation requires translocation of synaptically released Zn2+, J. Neurosci, 21, 8015, 10.1523/JNEUROSCI.21-20-08015.2001 Li, 2004, Characterization of NMDA induced depression in rat hippocampus, Neurosci. Lett, 357, 87, 10.1016/j.neulet.2003.11.004 Lin, 2000, Distinct molecular mechanisms and divergent endocytotic pathways of AMPA receptor internalization, Nat. Neurosci, 3, 1282, 10.1038/81814 Linden, 1997, Long-term potentiation of glial synaptic currents in cerebellar culture, Neuron, 18, 983, 10.1016/S0896-6273(00)80337-2 Linden, 1989, The role of protein kinase C in long-term potentiation, Brain Res. Brain Res. Rev, 14, 279, 10.1016/0165-0173(89)90004-0 Linden, 1991, A long-term depression of AMPA currents in cultured cerebellar Purkinje neurons, Neuron, 7, 81, 10.1016/0896-6273(91)90076-C Ling, 2002, Protein kinase Mzeta is necessary and sufficient for LTP maintenance, Nat. Neurosci, 5, 295, 10.1038/nn829 Lisman, 1989, A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory, Proc. Natl. Acad. Sci. USA, 86, 9574, 10.1073/pnas.86.23.9574 Lisman, 2003, Long-term potentiation, Philos. Trans. R. Soc. Lond. B Biol. Sci, 358, 829, 10.1098/rstb.2002.1242 Lisman, 1993, Quantal analysis and synaptic anatomy–integrating two views of hippocampal plasticity, Trends Neurosci, 16, 141, 10.1016/0166-2236(93)90122-3 Lisman, 2001, A model of synaptic memory, Neuron, 31, 191, 10.1016/S0896-6273(01)00364-6 Lisman, 2002, The molecular basis of CaMKII function in synaptic and behavioural memory, Nat. Rev. Neurosci, 3, 175, 10.1038/nrn753 Liu, 2004, Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity, Science, 304, 1021, 10.1126/science.1096615 Lonart, 2003, Phosphorylation of RIM1alpha by PKA triggers presynaptic long-term potentiation at cerebellar parallel fiber synapses, Cell, 115, 49, 10.1016/S0092-8674(03)00727-X Lüscher, 1999, Role of AMPA receptor cycling in synaptic transmission and plasticity, Neuron, 24, 649, 10.1016/S0896-6273(00)81119-8 Lüscher, 2000, Synaptic plasticity and dynamic modulation of the postsynaptic membrane, Nat. Neurosci, 3, 545, 10.1038/75714 Luthi, 1999, Hippocampal LTD expression involves a pool of AMPARs regulated by the NSF-GluR2 interaction, Neuron, 24, 389, 10.1016/S0896-6273(00)80852-1 Lynch, 2004, Long-term potentiation and memory, Physiol. Rev, 84, 87, 10.1152/physrev.00014.2003 Lynch, 1983, Intracellular injections of EGTA block induction of hippocampal long-term potentiation, Nature, 305, 719, 10.1038/305719a0 Malenka, 2003, The long-term potential of LTP, Nat. Rev. Neurosci, 4, 923, 10.1038/nrn1258 Malenka, 1993, NMDA-receptor-dependent synaptic plasticity, Trends Neurosci, 16, 521, 10.1016/0166-2236(93)90197-T Malenka, 1999, Long-term potentiation—a decade of progress?, Science, 285, 1870, 10.1126/science.285.5435.1870 Malenka, 1988, Postsynaptic calcium is sufficient for potentiation of hippocampal synaptic transmission, Science, 242, 81, 10.1126/science.2845577 Malenka, 1992, Temporal limits on the rise in postsynaptic calcium required for the induction of long-term potentiation, Neuron, 9, 121, 10.1016/0896-6273(92)90227-5 Malinow, 2002, AMPA receptor trafficking and synaptic plasticity, Annu. Rev. Neurosci, 25, 103, 10.1146/annurev.neuro.25.112701.142758 Malinow, 1989, Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP, Science, 245, 862, 10.1126/science.2549638 Malinow, 2000, LTP mechanisms, Curr. Opin. Neurobiol, 10, 352, 10.1016/S0959-4388(00)00099-4 Man, 2000, Regulation of AMPA receptor-mediated synaptic transmission by clathrin-dependent receptor internalization, Neuron, 25, 649, 10.1016/S0896-6273(00)81067-3 Man, 2003, Activation of PI3-kinase is required for AMPA receptor insertion during LTP of mEPSCs in cultured hippocampal neurons, Neuron, 38, 611, 10.1016/S0896-6273(03)00228-9 Manahan-Vaughan, 2000, Requirement of translation but not transcription for the maintenance of long-term depression in the CA1 region of freely moving rats, J. Neurosci, 20, 8572, 10.1523/JNEUROSCI.20-22-08572.2000 Mansvelder, 2000, Long-term potentiation of excitatory inputs to brain reward areas by nicotine, Neuron, 27, 349, 10.1016/S0896-6273(00)00042-8 Mato, 2004, A single in-vivo exposure to Delta 9THC blocks endocannabinoid-mediated synaptic plasticity, Nat. Neurosci, 7, 585, 10.1038/nn1251 Matsuzaki, 2004, Structural basis of long-term potentiation in single dendritic spines, Nature, 429, 761, 10.1038/nature02617 Matus, 2000, Actin-based plasticity in dendritic spines, Science, 290, 754, 10.1126/science.290.5492.754 Mellor, 2001, Hippocampal mossy fiber LTP is independent of postsynaptic calcium, Nat. Neurosci, 4, 125, 10.1038/83941 Mellor, 2002, Mediation of hippocampal mossy fiber long-term potentiation by presynaptic Ih channels, Science, 295, 143, 10.1126/science.1064285 Meng, 2003, Synaptic transmission and plasticity in the absence of AMPA glutamate receptor GluR2 and GluR3, Neuron, 39, 163, 10.1016/S0896-6273(03)00368-4 Minichiello, 2002, Mechanism of TrkB-mediated hippocampal long-term potentiation, Neuron, 36, 121, 10.1016/S0896-6273(02)00942-X Mizuno, 2001, Differential induction of LTP and LTD is not determined solely by instantaneous calcium concentration, Eur. J. Neurosci, 14, 701, 10.1046/j.0953-816x.2001.01679.x Mockett, 2002, NMDA receptor-mediated metaplasticity during the induction of long-term depression by low-frequency stimulation, Eur. J. Neurosci, 15, 1819, 10.1046/j.1460-9568.2002.02008.x Montgomery, 2002, State-dependent heterogeneity in synaptic depression between pyramidal cell pairs, Neuron, 33, 765, 10.1016/S0896-6273(02)00606-2 Monyer, 1992, Heteromeric NMDA receptors, Science, 256, 1217, 10.1126/science.256.5060.1217 Morishita, 2001, Regulation of synaptic strength by protein phosphatase 1, Neuron, 32, 1133, 10.1016/S0896-6273(01)00554-2 Mulkey, 1992, Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus, Neuron, 9, 967, 10.1016/0896-6273(92)90248-C Mulkey, 1993, An essential role for protein phosphatases in hippocampal long-term depression, Science, 261, 1051, 10.1126/science.8394601 Mulkey, 1994, Calcineurin and inhibitor-1 are components of a protein-phosphatase cascade mediating hippocampal LTD, Nature, 369, 486, 10.1038/369486a0 Nakano, 2004, Frequency-dependent requirement for calcium store-operated mechanisms in induction of homosynaptic long-term depression at hippocampus CA1 synapses, Eur. J. Neurosci, 19, 2881, 10.1111/j.0953-816X.2004.03390.x Nestler, 2001, Molecular basis of long-term plasticity underlying addiction, Nat. Rev. Neurosci, 2, 119, 10.1038/35053570 Neves, 2002, Modeling of signaling networks, Bioessays, 24, 1110, 10.1002/bies.1154 Ngezahayo, 2000, Synaptic activity modulates the induction of bidirectional synaptic changes in adult mouse hippocampus, J. Neurosci, 20, 2451, 10.1523/JNEUROSCI.20-07-02451.2000 Nicoll, 1995, Contrasting properties of two forms of long-term potentiation in the hippocampus, Nature, 377, 115, 10.1038/377115a0 Nicoll, 1999, Expression mechanisms underlying NMDA receptor-dependent long-term potentiation, Ann. N Y Acad. Sci, 868, 515, 10.1111/j.1749-6632.1999.tb11320.x Nishimune, 1998, NSF binding to GluR2 regulates synaptic transmission, Neuron, 21, 87, 10.1016/S0896-6273(00)80517-6 Nishiyama, 2000, Calcium stores regulate the polarity and input specificity of synaptic modification, Nature, 408, 584, 10.1038/35046067 Oliet, 1997, Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells, Neuron, 18, 969, 10.1016/S0896-6273(00)80336-0 Otto, 2001, Impairment of mossy fiber long-term potentiation and associative learning in pituitary adenylate cyclase activating polypeptide type I receptor-deficient mice, J. Neurosci, 21, 5520, 10.1523/JNEUROSCI.21-15-05520.2001 Palmer, 1997, The group I mGlu receptor agonist DHPG induces a novel form of LTD in the CA1 region of the hippocampus, Neuropharmacology, 36, 1517, 10.1016/S0028-3908(97)00181-0 Patrick, 2003, Ubiquitin-mediated proteasome activity is required for agonist-induced endocytosis of GluRs, Curr. Biol, 13, 2073, 10.1016/j.cub.2003.10.028 Philpot, 2002, Synaptic plasticity in an altered state, Neuron, 33, 665, 10.1016/S0896-6273(02)00618-9 Pittenger, 2003, In search of general mechanisms for long-lasting plasticity, Philos. Trans. R. Soc. Lond. B Biol. Sci, 358, 757, 10.1098/rstb.2002.1247 Poo, 2001, Neurotrophins as synaptic modulators, Nat. Rev. Neurosci, 2, 24, 10.1038/35049004 Quinlan, 1999, Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo, Nat. Neurosci, 2, 352, 10.1038/7263 Rammes, 2003, Activation of mGlu receptors induces LTD without affecting postsynaptic sensitivity of CA1 neurons in rat hippocampal slices, J. Physiol, 546, 455, 10.1113/jphysiol.2002.033514 Regehr, 1991, The maintenance of LTP at hippocampal mossy fiber synapses is independent of sustained presynaptic calcium, Neuron, 7, 451, 10.1016/0896-6273(91)90297-D Reid, 2004, Optical quantal analysis indicates that long-term potentiation at single hippocampal mossy fiber synapses is expressed through increased release probability, recruitment of new release sites, and activation of silent synapses, J. Neurosci, 24, 3618, 10.1523/JNEUROSCI.3567-03.2004 Rittenhouse, 1999, Monocular deprivation induces homosynaptic long-term depression in visual cortex, Nature, 397, 347, 10.1038/16922 Robbe, 2002, Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens, Proc. Natl. Acad. Sci. USA, 99, 8384, 10.1073/pnas.122149199 Roberts, 1998, Suppression of NMDA receptor function using antisense DNA block ocular dominance plasticity while preserving visual responses, J. Neurophysiol, 80, 1021, 10.1152/jn.1998.80.3.1021 Saal, 2003, Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons, Neuron, 37, 577, 10.1016/S0896-6273(03)00021-7 Sajikumar, 2003, Anisomycin inhibits the late maintenance of long-term depression in rat hippocampal slices in vitro, Neurosci. Lett, 338, 147, 10.1016/S0304-3940(02)01400-3 Salin, 1996, Cyclic AMP mediates a presynaptic form of LTP at cerebellar parallel fiber synapses, Neuron, 16, 797, 10.1016/S0896-6273(00)80099-9 Salter, 2004, Src kinases, Nat. Rev. Neurosci, 5, 317, 10.1038/nrn1368 Sanes, 1999, Can molecules explain long-term potentiation?, Nat. Neurosci, 2, 597, 10.1038/10154 Sawtell, 1999, Induction of NMDA receptor-dependent long-term depression in visual cortex does not require metabotropic glutamate receptors, J. Neurophysiol, 82, 3594, 10.1152/jn.1999.82.6.3594 Scheiderer, 2004, Novel form of long-term synaptic depression in rat hippocampus induced by activation of alpha 1 adrenergic receptors, J. Neurophysiol, 91, 1071, 10.1152/jn.00420.2003 Schlüter, 1999, Rabphilin knock-out mice reveal that rabphilin is not required for rab3 function in regulating neurotransmitter release, J. Neurosci, 19, 5834, 10.1523/JNEUROSCI.19-14-05834.1999 Schmitz, 2003, Presynaptic kainate receptors impart an associative property to hippocampal mossy fiber long-term potentiation, Nat. Neurosci, 6, 1058, 10.1038/nn1116 Schnell, 2002, Direct interactions between PSD-95 and stargazin control synaptic AMPA receptor number, Proc. Natl. Acad. Sci. USA, 99, 13902, 10.1073/pnas.172511199 Seidenman, 2003, Glutamate receptor subunit 2 Serine 880 phosphorylation modulates synaptic transmission and mediates plasticity in CA1 pyramidal cells, J. Neurosci, 23, 9220, 10.1523/JNEUROSCI.23-27-09220.2003 Selig, 1995, Independent mechanisms for long-term depression of AMPA and NMDA responses, Neuron, 15, 417, 10.1016/0896-6273(95)90045-4 Shen, 1999, Dynamic control of CaMKII translocation and localization in hippocampal neurons by NMDA receptor stimulation, Science, 284, 162, 10.1126/science.284.5411.162 Sheng, 2001, Molecular organization of the postsynaptic specialization, Proc. Natl. Acad. Sci. USA, 98, 7058, 10.1073/pnas.111146298 Sheng, 2003, AMPA receptor trafficking and synaptic plasticity, Neurosci. Res, 46, 127, 10.1016/S0168-0102(03)00040-3 Shi, 2001, Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons, Cell, 105, 331, 10.1016/S0092-8674(01)00321-X Shigemoto, 1994, Antibodies inactivating mGluR1 metabotropic glutamate receptor block long-term depression in cultured Purkinje cells, Neuron, 12, 1245, 10.1016/0896-6273(94)90441-3 Silva, 1998, CREB and memory, Annu. Rev. Neurosci, 21, 127, 10.1146/annurev.neuro.21.1.127 Sjostrom, 2003, Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors, Neuron, 39, 641, 10.1016/S0896-6273(03)00476-8 Sjostrom, P.J., Turrigiano, G.G., and Nelson, S.B. (2004). Endocannabinoid-dependent neocortical layer-5 LTD in the absence of postsynaptic spiking. J. Neurophysiol., in press. Published online July 7, 2004. 0: 3762004-0. Slepnev, 1998, Role of phosphorylation in regulation of the assembly of endocytic coat complexes, Science, 281, 821, 10.1126/science.281.5378.821 Snyder, 2001, Internalization of ionotropic glutamate receptors in response to mGluR activation, Nat. Neurosci, 4, 1079, 10.1038/nn746 Soderling, 2000, Postsynaptic protein phosphorylation and LTP, Trends Neurosci, 23, 75, 10.1016/S0166-2236(99)01490-3 Song, 2002, Regulation of AMPA receptors during synaptic plasticity, Trends Neurosci, 25, 578, 10.1016/S0166-2236(02)02270-1 Song, 1998, Interaction of the N-ethylmaleimide-sensitive factor with AMPA receptors, Neuron, 21, 393, 10.1016/S0896-6273(00)80548-6 Spillane, 1995, Long-term potentiation in mice lacking synapsins, Neuropharmacology, 34, 1573, 10.1016/0028-3908(95)00107-H Staubli, 1990, Stable depression of potentiated synaptic responses in the hippocampus with 1–5 Hz stimulation, Brain Res, 513, 113, 10.1016/0006-8993(90)91096-Y Stent, 1973, A physiological mechanism for Hebb's postulate of learning, Proc. Natl. Acad. Sci. USA, 70, 997, 10.1073/pnas.70.4.997 Steward, 2001, Protein synthesis at synaptic sites on dendrites, Annu. Rev. Neurosci, 24, 299, 10.1146/annurev.neuro.24.1.299 Sudhof, 2001, The synaptic cleft and synaptic cell adhesion, 275 Sudhof, 2004, The synaptic vesicle cycle, Annu. Rev. Neurosci, 27, 509, 10.1146/annurev.neuro.26.041002.131412 Sudhof, 1989, Synapsins, Science, 245, 1474, 10.1126/science.2506642 Sung, 2001, Activation of group I mGluRs is necessary for induction of long-term depression at striatal synapses, J. Neurophysiol, 86, 2405, 10.1152/jn.2001.86.5.2405 Sutton, 2003, Extinction-induced upregulation in AMPA receptors reduces cocaine-seeking behaviour, Nature, 421, 70, 10.1038/nature01249 Sweatt, 2004, Mitogen-activated protein kinases in synaptic plasticity and memory, Curr. Opin. Neurobiol, 14, 311, 10.1016/j.conb.2004.04.001 Takahashi, 2003, Experience strengthening transmission by driving AMPA receptors into synapses, Science, 299, 1585, 10.1126/science.1079886 Tan, 2003, The mechanism of presynaptic long-term depression mediated by group I metabotropic glutamate receptors, Cell. Mol. Neurobiol, 23, 187, 10.1023/A:1022949922364 Tang, 1999, Genetic enhancement of learning and memory in mice, Nature, 401, 63, 10.1038/43432 Terashima, 2004, Regulation of synaptic strength and AMPA receptor subunit composition by PICK1, J. Neurosci, 24, 5381, 10.1523/JNEUROSCI.4378-03.2004 Thiels, 1996, NMDA receptor-dependent LTD in different subfields of hippocampus in vivo and in vitro, Hippocampus, 6, 43, 10.1002/(SICI)1098-1063(1996)6:1<43::AID-HIPO8>3.0.CO;2-8 Thiels, 2002, Long-term depression in the adult hippocampus in vivo involves activation of extracellular signal-regulated kinase and phosphorylation of Elk-1, J. Neurosci, 22, 2054, 10.1523/JNEUROSCI.22-06-02054.2002 Thomas, 2004, MAPK cascade signalling and synaptic plasticity, Nat. Rev. Neurosci, 5, 173, 10.1038/nrn1346 Thomas, 2003, Synaptic plasticity in the mesolimbic dopamine system, Philos. Trans. R. Soc. Lond. B Biol. Sci, 358, 815, 10.1098/rstb.2002.1236 Thomas, 2001, Long-term depression in the nucleus accumbens, Nat. Neurosci, 4, 1217, 10.1038/nn757 Tong, 1996, Long-term potentiation in cultures of single hippocampal granule cells, Neuron, 16, 1147, 10.1016/S0896-6273(00)80141-5 Turrigiano, 2004, Homeostatic plasticity in the developing nervous system, Nat. Rev. Neurosci, 5, 97, 10.1038/nrn1327 Ungless, 2001, Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons, Nature, 411, 583, 10.1038/35079077 van Dam, 2002, N-methyl-D-aspartate-induced long-term depression is associated with a decrease in postsynaptic protein kinase C substrate phosphorylation in rat hippocampal slices, Neurosci. Lett, 320, 129, 10.1016/S0304-3940(02)00037-X Vanderschuren, 2000, Alterations in dopaminergic and glutamatergic transmission in the induction and expression of behavioral sensitization, Psychopharmacology (Berl.), 151, 99, 10.1007/s002130000493 Vekovischeva, 2001, Morphine-induced dependence and sensitization are altered in mice deficient in AMPA-type glutamate receptor-A subunits, J. Neurosci, 21, 4451, 10.1523/JNEUROSCI.21-12-04451.2001 Villacres, 1998, Type I adenylyl cyclase mutant mice have impaired mossy fiber long-term potentiation, J. Neurosci, 18, 3186, 10.1523/JNEUROSCI.18-09-03186.1998 Wang, 2000, Expression of cerebellar long-term depression requires postsynaptic clathrin-mediated endocytosis, Neuron, 25, 635, 10.1016/S0896-6273(00)81066-1 Wang, 2003, Type 8 adenylyl cyclase is targeted to excitatory synapses and required for mossy fiber long-term potentiation, J. Neurosci, 23, 9710, 10.1523/JNEUROSCI.23-30-09710.2003 Watabe, 2002, Postsynaptic induction and presynaptic expression of group 1 mGluR-dependent LTD in the hippocampal CA1 region, J. Neurophysiol, 87, 1395, 10.1152/jn.00723.2001 Weisskopf, 1995, Presynaptic changes during mossy fibre LTP revealed by NMDA receptor- mediated synaptic responses, Nature, 376, 256, 10.1038/376256a0 Williams, 1993, The search for retrograde messengers in long-term potentiation, Sem. Neurosci, 5, 149, 10.1016/S1044-5765(05)80048-X Williams, 1998, Biphasic changes in the levels of N-methyl-D-aspartate receptor-2 subunits correlate with the induction and persistence of long-term potentiation, Brain Res. Mol. Brain Res, 60, 21, 10.1016/S0169-328X(98)00154-5 Williams, 2003, Long-term regulation of N-methyl-D-aspartate receptor subunits and associated synaptic proteins following hippocampal synaptic plasticity, Neuroscience, 118, 1003, 10.1016/S0306-4522(03)00028-9 Wilson, 2002, Endocannabinoid signaling in the brain, Science, 296, 678, 10.1126/science.1063545 Wu, 2004, Synaptically stimulated induction of group I metabotropic glutamate receptor-dependent long-term depression and depotentiation is inhibited by prior activation of metabotropic glutamate receptors and protein kinase C, Neuroscience, 123, 507, 10.1016/j.neuroscience.2003.09.013 Xiao, 1994, Long-term depression in the hippocampal CA1 region is associated with equal changes in AMPA and NMDA receptor-mediated synaptic potentials, Eur. J. Neurosci, 6, 1055, 10.1111/j.1460-9568.1994.tb00600.x Xiao, 1995, On the linkage between AMPA and NMDA receptor-mediated EPSPs in homosynaptic long-term depression in the hippocampal CA1 region of young rats, J. Neurosci, 15, 4496, 10.1523/JNEUROSCI.15-06-04496.1995 Xiao, 2001, Metabotropic glutamate receptor activation causes a rapid redistribution of AMPA receptors, Neuropharmacology, 41, 664, 10.1016/S0028-3908(01)00134-4 Yang, 1999, Selective induction of LTP and LTD by postsynaptic [Ca2+]i elevation, J. Neurophysiol, 81, 781, 10.1152/jn.1999.81.2.781 Yasuda, 2003, A developmental switch in the signaling cascades for LTP induction, Nat. Neurosci, 6, 15, 10.1038/nn985 Yeckel, 1999, Multiple forms of LTP in hippocampal CA3 neurons use a common postsynaptic mechanism, Nat. Neurosci, 2, 625, 10.1038/10180 Yuste, 2001, Morphological changes in dendritic spines associated with long-term synaptic plasticity, Annu. Rev. Neurosci, 24, 1071, 10.1146/annurev.neuro.24.1.1071 Zakharenko, 2002, Altered presynaptic vesicle release and cycling during mGluR-dependent LTD, Neuron, 35, 1099, 10.1016/S0896-6273(02)00898-X Zakharenko, 2003, Presynaptic BDNF required for a presynaptic but not postsynaptic component of LTP at hippocampal CA1–CA3 synapses, Neuron, 39, 975, 10.1016/S0896-6273(03)00543-9 Zalutsky, 1990, Comparison of two forms of long-term potentiation in single hippocampal neurons, Science, 248, 1619, 10.1126/science.2114039 Zamanillo, 1999, Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning, Science, 284, 1805, 10.1126/science.284.5421.1805 Zhang, 2003, The other side of the engram, Nat. Rev. Neurosci, 4, 885, 10.1038/nrn1248 Zhao, 2004, Extracellular signal-regulated kinase 1/2 is required for the induction of group I metabotropic glutamate receptor-mediated epileptiform discharges, J. Neurosci, 24, 76, 10.1523/JNEUROSCI.4515-03.2004 Zho, 2002, The group I metabotropic glutamate receptor agonist (S)-3,5-dihydroxyphenylglycine induces a novel form of depotentiation in the CA1 region of the hippocampus, J. Neurosci, 22, 8838, 10.1523/JNEUROSCI.22-20-08838.2002 Zhu, 2002, Ras and Rap control AMPA receptor trafficking during synaptic plasticity, Cell, 110, 443, 10.1016/S0092-8674(02)00897-8