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Endocannabinoid Signaling in Neural Plasticity

  • Bradley E. AlgerEmail author
Chapter
Part of the Current Topics in Behavioral Neurosciences book series (CTBN, volume 1)

Abstract

Plasticity refers to a physiologically measured change that may last for short or long periods of time. Endocannabinoids (ECBs) are prevalent throughout most of the brain, and modulate synaptic transmission in many ways. This chapter will focus on the roles of ECBs in neural plasticity in the mammalian brain. The topics covered can be divided loosely into two themes: how ECBs regulate synaptic plasticity, and how ECBs’ actions themselves are regulated by neuronal activity. Because ECBs regulate synaptic plasticity, the modifiability of ECB mobilization constitutes a form of “metaplasticity” (as reported by Abraham and Bear (Trends Neurosci 19:126–130, 1996)), i.e., an upstream process that determines the nature and extent of synaptic plasticity. Many of their basic functions are still being discovered, and while there is consensus on large issues, many points of divergence exist as well. This chapter concentrates on developments in the roles of ECBs in synaptic plasticity that have come to light since the major review by Chevaleyre et al. (Annu Rev Neurosci 29:37–76, 2006).

Keywords

DSI DSE LTD iLTD Inhibition Seizure 

References

  1. Abraham WC, Bear MF (1996) Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci 19:126–130PubMedGoogle Scholar
  2. Abraham WC, Gustafsson B, Wigstrom H (1987) Long-term potentiation involves enhanced synaptic excitation relative to synaptic inhibition in guinea-pig hippocampus. J Physiol (Lond) 394:367–380Google Scholar
  3. Adermark L, Lovinger DM (2007a) Combined activation of L-type Ca2+ channels and synaptic transmission is sufficient to induce striatal long-term depression. J Neurosci 27:6781–6787PubMedGoogle Scholar
  4. Ade KK, Lovinger DM (2007) Anandamide regulates postnatal development of long-term synaptic plasticity in the rat dorsolateral striatum. J Neurosci 27(9):2403–2409.PubMedGoogle Scholar
  5. Adermark L, Lovinger DM (2007b) Retrograde endocannabinoid signaling at striatal synapses requires a regulated postsynaptic release step. Proc Natl Acad Sci USA 104:20564–20569PubMedGoogle Scholar
  6. Alger BE (2002) Retrograde signaling in the regulation of synaptic transmission: focus on endocannabinoids. Prog Neurobiol 68:247–286PubMedGoogle Scholar
  7. Alger BE, Pitler TA (1995) Retrograde signaling at GABAA-receptor synapses in the mammalian CNS. Trends Neurosci 18:333–340PubMedGoogle Scholar
  8. Alger BE, Pitler TA, Wagner JJ et al. (1996) Retrograde signalling in depolarization-induced suppression of inhibition in rat hippocampal CA1 cells. J Physiol (Lond) 496:197–209Google Scholar
  9. Ali AB (2007) Presynaptic inhibition of GABAA receptor mediated unitary IPSPs by cannabinoid receptors at synapses between CCK-positive interneurons in rat hippocampus. J Neurophysiol 98:861–869PubMedGoogle Scholar
  10. Azad SC, Monory K, Marsicano G et al. (2004) Circuitry for associative plasticity in the amygdala involves endocannabinoid signaling. J Neurosci 24:9953–9961PubMedGoogle Scholar
  11. Azad SC, Kurz J, Marsicano G et al. (2008) Activation of CB1 specifically located on GABAergic interneurons inhibits LTD in the lateral amygdala. Learn Memory 15:143–152Google Scholar
  12. Bacci A, Huguenard JR, Prince DA (2004) Long-lasting self-inhibition of neocortical interneurons mediated by endocannabinoids. Nature 431:312–316PubMedGoogle Scholar
  13. Bean BP (1989) Neurotransmitter inhibition of neuronal calcium currents by changes in channel voltage dependence. Nature 340:153–156PubMedGoogle Scholar
  14. Beierlein M, Regehr WG (2006) Local interneurons regulate synaptic strength by retrograde release of endocannabinoids. J Neurosci 26:9935–9943PubMedGoogle Scholar
  15. Beierlein M, Fioravante D, Regehr WG (2007) Differential expression of posttetanic potentiation and retrograde signaling mediate target-dependent short-term synaptic plasticity. Neuron 54:949–959PubMedGoogle Scholar
  16. Bender VA, Bender KJ, Brasier DJ et al. (2008) Two coincidence detectors for spike timingdependent plasticity in somatosensory cortex. J Neurosci 26:4166–4177Google Scholar
  17. Bliss TV, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol (Lond) 232:331–356Google Scholar
  18. Bouaboula M, Perrachon S, Milligan L et al. (1997) A selective inverse agonist for central cannabinoid receptor inhibits mitogen-activated protein kinase activation stimulated by insulin or insulin-like growth factor 1. Evidence for a new model of receptor/ligand interactions. J Biol Chem 272:22330–22339PubMedGoogle Scholar
  19. Brenowitz SD, Regehr WG (2003) Calcium dependence of retrograde inhibition by endocannabinoids at synapses onto Purkinje cells. J Neurosci 23:6373–6384PubMedGoogle Scholar
  20. Brenowitz SD, Best AR, Regehr WG (2006) Sustained elevation of dendritic calcium evokes widespread endocannabinoid release and suppression of synapses onto cerebellar Purkinje cells. J Neurosci 26:6841–6850PubMedGoogle Scholar
  21. Brown SP, Brenowitz SD, Regehr WG (2003) Brief presynaptic bursts evoke synapse-specific retrograde inhibition mediated by endogenous cannabinoids. Nat Neurosci 6:1048–1057PubMedGoogle Scholar
  22. Brown SP, Safo PK, Regehr WG (2004) Endocannabinoids inhibit transmission at granule cell to Purkinje cell synapses by modulating three types of presynaptic calcium channels. J Neurosci 24:5623–5631PubMedGoogle Scholar
  23. Brown SP, Brenowitz SD, Regehr W (2003) Brief presynaptic bursts evoke synapse-specific retrograde inhibition mediated by endogenous cannabinoids. Nat Neurosci 6:1048–1057PubMedGoogle Scholar
  24. Carlson G, Wang Y, Alger BE (2002) Endocannabinoids facilitate the induction of LTP in the hippocampus. Nat Neurosci 5:723–724PubMedGoogle Scholar
  25. Castillo PE, Schoch S, Schmitz F et al. (2002) RIM1α is required for presynaptic long-term potentiation. Nature 415:327–330PubMedGoogle Scholar
  26. Chen K, Ratzliff A, Hilgenberg L et al. (2003) Long-term plasticity of endocannabinoid signaling induced by developmental febrile seizures. Neuron 39:599–611PubMedGoogle Scholar
  27. Chen K, Neu A, Howard AL et al. (2007) Prevention of plasticity of endocannabinoid signalling inhibits persistent limbic hyperexcitability caused by developmental seizures. J Neurosci 27:46–58PubMedGoogle Scholar
  28. Chevaleyre V, Castillo PE (2003) Heterosynaptic LTD of hippocampal GABAergic synapses. A novel role of endocannabinoids in regulating excitability. Neuron 38:461–472PubMedGoogle Scholar
  29. Chevaleyre V, Castillo PE (2004) Endocannabinoid-mediated metaplasticity in the hippocampus. Neuron 43:871–881PubMedGoogle Scholar
  30. Chevaleyre V, Takahashi KA, Castillo PE (2006) Endocannabinoid-mediated synaptic plasticity in the CNS. Annu Rev Neurosci 29:37–76PubMedGoogle Scholar
  31. Chevaleyre V, Heifets BD, Kaeser PS et al. (2007) Endocannabinoid-mediated long-term plasticity requires cAMP/PKA signaling and RIM1α. Neuron 54:801–812PubMedGoogle Scholar
  32. Crozier RA, Wang Y, Liu C-H et al. (2007) Deprivation-induced synaptic depression by distinct mechanisms in different layers of mouse visual cortex. Proc Natl Acad Sci USA 104:1383–1388PubMedGoogle Scholar
  33. Dan Y, Poo M (2004) Spike timing-dependent plasticity of neural circuits. Neuron 44:23–30PubMedGoogle Scholar
  34. Deadwyler SA, Hampson RE, Mu J et al. (1995) Cannabinoids modulate voltage sensitive potassium A-current in hippocampal neurons via a cAMP-dependent process. J Pharmacol Exp Ther 273:734–743PubMedGoogle Scholar
  35. Di S, Malcher-Lopes R, Marcheselli VL et al. (2005) Rapid glucocorticoid-mediated endocannabinoid release and opposing regulation of glutamate and gamma-aminobutyric acid inputs to hypothalamic magnocellular neurons. Endocrinology 145:4292–4301Google Scholar
  36. Diana MA, Marty A (2003) Characterization of depolarization-induced suppression of inhibition using paired interneuron – Purkinje cell recordings. J Neurosci 23:5906–5918PubMedGoogle Scholar
  37. Dinh TP, Freund TF, Piomelli D (2002) A role for monoglyceride lipase in 2-arachidonoylglycerol inactivation. Chem Phys Lipids 121:149–158PubMedGoogle Scholar
  38. Edwards DA, Kim J, Alger BE (2006) Multiple mechanisms of endocannabinoid response initiation in hippocampus. J Neurophysiol 95:67–75PubMedGoogle Scholar
  39. Edwards DA, Zhang L, Alger BE (2008) Metaplastic control of the endocannabinoid system at inhibitory synapses in hippocampus. Proc Natl Acad Sci USA 105:8142–8147PubMedGoogle Scholar
  40. Foldy C, Neu A, Jones MV et al. (2006) Presynaptic, activity-dependent modulation of cannabinoid type 1 receptor-mediated inhibition of GABA release. J Neurosci 26:1465–1469PubMedGoogle Scholar
  41. Foldy C, Lee SY, Szabadics J et al. (2007) Cell type-specific gating of perisomatic inhibition by cholecystokinin. Nature Neurosci 10:1128–1130PubMedGoogle Scholar
  42. Fortin DA, Levine ES (2007) Differential effects of endocannabinoids on glutamatergic and GABAergic inputs to layer 5 pyramidal neurons. Cereb Cortex 17:163–174PubMedGoogle Scholar
  43. Fortin DA, Trettel J, Levine ES (2004) Brief trains of action potentials enhance pyramidal neuron excitability via endocannabinoid-mediated suppression of inhibition. J Neurophysiol 92:2105–2112PubMedGoogle Scholar
  44. Freund TF, Katona I, Piomelli D (2003) Role of endogenous cannabinoids in synaptic signaling. Physiol Rev 83:1017–1066PubMedGoogle Scholar
  45. Gerdeman G, Lovinger DM (2001) CB1 cannabinoid receptor inhibits synaptic release of glutamate in rat dorsolateral striatum. J Neurophysiol 85:468–471PubMedGoogle Scholar
  46. Gerdeman GL, Ronesi J, Lovinger DM (2002) Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nature Neurosci 5:446–451PubMedGoogle Scholar
  47. Gibson HE, Edwards JG, Page RS et al. (2008) TRPV1 channels mediate long-term depression at synapses on hippocampal interneurons. Neuron 57:746–759PubMedGoogle Scholar
  48. Giuffrida A, Parsons LH, Kerr TM et al. (1999) Dopamine activation of endogenous cannabinoid signaling in dorsal striatum. Nature Neurosci 2:358–363PubMedGoogle Scholar
  49. Gubellini P, Pisani A, Centonze D et al. (2004) Metabotropic glutamate receptors and striatal synaptic plasticity: implications for neurological diseases. Prog Neurobiol 74:271–300PubMedGoogle Scholar
  50. Hampson RE, Zhuang SY, Weiner JL et al. (2003) Functional significance of cannabinoid-mediated, depolarization induced suppression of inhibition (DSI) in the hippocampus. J Neurophysiol 90:55–64PubMedGoogle Scholar
  51. Hashimotodani Y, Ohno-Shosaku T, Tsubokawa H et al. (2005) Phospholipase Cβ serves as a coincidence detector through its Ca2+ dependency for triggering retrograde endocannabinoid signal. Neuron 45:257–268PubMedGoogle Scholar
  52. Hashimotodani Y, Ohno-Shosaku T, Kano M (2007) Presynaptic monoacylglycerol lipase activity determines basal endocannabinoid tone and terminates retrograde endocannabinoid signaling in the hippocampus. J Neurosci 27:1211–1219PubMedGoogle Scholar
  53. Heinbockel T, Brager DH, Reich CG et al. (2005) Endocannabinoid signaling dynamics probed with optical tools. J Neurosci 25:9449–9459PubMedGoogle Scholar
  54. Hentges ST, Low MJ, Williams JT (2005) Differential regulation of synaptic inputs by constitutively released endocannabinoids and exogenous cannabinoids. J Neurosci 25:9746–9751PubMedGoogle Scholar
  55. Hirasawa M, Schwab Y, Natah S et al. (2004) Dendritically released transmitters cooperate via autocrine and retrograde actions to inhibit afferent excitation in rat brain. J Physiol (Lond) 559:611–624Google Scholar
  56. Hoffman AF, Lupica CR (2000) Mechanisms of cannabinoid inhibition of GABAA synaptic transmission in the hippocampus. J Neurosci 20:2470–2479PubMedGoogle Scholar
  57. Hoffman AF, Riegel AC, Lupica CR (2003) Functional localization of cannabinoid receptors and endogenous cannabinoid production in distinct neuron populations of the hippocampus. Eur J Neurosci 18:524–534PubMedGoogle Scholar
  58. Ikeda SR (1991) Double-pulse calcium channel current facilitation in adult rat sympathetic neurones. J Physiol (Lond) 439:181–214Google Scholar
  59. Isokawa M, Alger BE (2006) Ryanodine receptor regulates endogenous cannabinoid mobilization in the hippocampus. J Neurophysiol 95:3001–3011PubMedGoogle Scholar
  60. Ito M (2001) Cerebellar long-term depression: characterization, signal transduction, and functional roles. Physiol Rev 81:1143–1195PubMedGoogle Scholar
  61. Kawamura Y, Fukaya M, Maejima T et al. (2006) The CB1 cannabinoid receptor is the major cannabinoid receptor at excitatory presynaptic sites in the hippocampus and cerebellum. J Neurosci 26:2991–3001PubMedGoogle Scholar
  62. Kim J, Isokawa M, Ledent C et al. (2002) Activation of muscarinic acetylcholine receptors enhances the release of endogenous cannabinoids in the hippocampus. J Neurosci 22:10182–10191PubMedGoogle Scholar
  63. Klapstein GJ, Colmers WF (1992) 4-Aminopyridine and low Ca2+ differentiate presynaptic inhibition mediated by neuropeptide Y, baclofen and 2-chloroadenosine in rat hippocampal CA1 in vitro. Br J Pharmacol 105:470–474PubMedGoogle Scholar
  64. Kombian SB, Mouginot D, Pittman QJ (1997) Dendritically released peptides act as retrograde modulators of afferent excitation in the supraoptic nucleus in vitro. Neuron 19:903–912PubMedGoogle Scholar
  65. Kreitzer AC, Malenka RC (2005) Dopamine modulation of state-dependent endocannabinoid release and long-term depression in the striatum. J Neurosci 25:10537–10545PubMedGoogle Scholar
  66. Kreitzer AC, Regehr WG (2001) Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29:717–727PubMedGoogle Scholar
  67. Kreitzer AC, Carter AG, Regehr WG (2002) Inhibition of interneuron firing extends the spread of endocannabinoid signaling in the cerebellum. Neuron 34:787–796PubMedGoogle Scholar
  68. Lenz RA, Wagner JJ, Alger BE (1998) N- and L-type calcium channel involvement in depolarization-induced suppression of inhibition in rat hippocampal CA1 cells. J Physiol (Lond) 512:61–73Google Scholar
  69. Liu C-H, Heynen AJ, Schuler MG et al. (2008) Cannabinoid receptor blockade reveals parallel plasticity mechanisms in different layers of mouse visual cortex. Neuron 58:340–345PubMedGoogle Scholar
  70. Llano I, Leresche N, Marty A (1991) Calcium entry increases the sensitivity of cerebellar Purkinje cells to applied GABA and decreases inhibitory synaptic currents. Neuron 6:565–574PubMedGoogle Scholar
  71. Losonczy A, Biro AA, Nusser Z (2004) Persistently active cannabinoid receptors mute a sub-population of hippocampal interneurons. Proc Natl Acad Sci USA 101:1362–1367PubMedGoogle Scholar
  72. Maccarrone M, Rossi S, Bari M et al. (2008) Anandamide inhibits metabolism and physiological actions of 2-arachidonoyglycerol in the striatum. Nature Neurosci 11:152–159PubMedGoogle Scholar
  73. Maejima T, Hasimoto K, Yoshida T et al. (2001) Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabinoid receptors. Neuron 31:463–475PubMedGoogle Scholar
  74. Maejima T, Oka S, Hashimotodani Y et al. (2005) Synaptically driven endocannabinoid release requires Ca2 + -assisted metabotropic glutamate receptor subtype 1 to phospholipase C β4 signaling cascade in the cerebellum. J Neurosci 25:6826–6835PubMedGoogle Scholar
  75. Makara JK, Katona I, Nyiri G et al. (2007) Involvement of nitric oxide in depolarization-induced suppression of inhibition in hippocampal pyramidal cells during activation of cholinergic receptors. J Neurosci 27:10211–10222PubMedGoogle Scholar
  76. Marcaggi P, Attwell D (2005) Endocannabinoid signaling depends on the spatial pattern of synapse activation. Nat Neurosci 8:776–781PubMedGoogle Scholar
  77. Marsicano G, Wotjak CT, Azad SC et al. (2002) The endogenous cannabinoid system controls extinction of aversive memories. Nature 418:530–534PubMedGoogle Scholar
  78. Marsicano G, Goodenough S, Monory K et al. (2003) CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 302:84–88PubMedGoogle Scholar
  79. Melis M, Perra S, Muntoni AL et al. (2004a) Prefrontal cortex stimulation induces 2-arachidonoyl-glycerol-mediated suppression of excitation in dopamine neurons. J Neurosci 24:10707–10715PubMedGoogle Scholar
  80. Melis M, Pistis M, Perra S et al. (2004b) Endocannabinoids mediate presynaptic inhibition of glutamatergic transmission in rat ventral tegmental area dopamine neurons through activation of CB1 receptors. J Neurosci 24:53–62PubMedGoogle Scholar
  81. Monory K, Massa F, Egertova M et al. (2006) The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron 51:455–466PubMedGoogle Scholar
  82. Mu J, Zhuang S-Y, Hampson RE et al. (2000) Protein kinase-dependent phosphorylation and cannabinoid receptor modulation of potassium A current (IA) in cultured rat hippocampal neurons. Pflugers Arch 439:541–546PubMedGoogle Scholar
  83. Mukhtarov M, Ragozzino D, Bregestovski P (2005) Dual Ca2+ modulation of glycinergic synaptic currents in rodent hypoglossal motoneurones. J Physiol (Lond) 569:817–831Google Scholar
  84. Neu A, Foldy C, Soltesz I (2007) Postsynaptic origin of CB1-dependent tonic inhibition of GABA release at CCK-positive basket cell to pyramidal cell synapses in the CA1 region of the rat hippocampus. J Physiol (Lond) 578:233–247Google Scholar
  85. Nevian T, Sakmann B (2006) Spine Ca2+ signalling in spike-timing-dependent plasticity. J Neurosci 26:11001–11013PubMedGoogle Scholar
  86. Ohno-Shosaku T, Maejima T, Kano M (2001) Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 29:729–738PubMedGoogle Scholar
  87. Ohno-Shosaku T, Tsubokawa H, Mizushima I et al. (2002) Presynaptic cannabinoid sensitivity is a major determinant of depolarization-induced retrograde suppression at hippocampal synapses. J Neurosci 22:3864–3872PubMedGoogle Scholar
  88. Ohno-Shosaku T, Matsui M, Fukudome Y et al. (2003) Postsynaptic M1 and M3 receptors are responsible for the muscarinic enhancement of retrograde endocannabinoid signalling in the hippocampus. Eur J Neurosci 18:109–116PubMedGoogle Scholar
  89. Ohno-Shosaku T, Hashimotodani Y, Ano M et al. (2007) Endocannabinoid signaling triggered by NMDA receptor-mediated calcium entry into rat hippocampal neurons. J Physiol (Lond) 584:407–418Google Scholar
  90. Oliet SHR, Baimoukhametova DV, Piet R et al. (2007) Retrograde regulation of GABA transmission by the tonic release of oxytocin and endocannabinoids governs postsynaptic firing. J Neurosci 27:1325–1333PubMedGoogle Scholar
  91. Pan B, Hillard CJ, Liu QS (2008) Endocannabinoid signaling mediates cocaine-induced inhibitory synaptic plasticity in midbrain dopamine neurons. J Neurosci 28:1385–1397PubMedGoogle Scholar
  92. Pertwee RG (2005) Inverse agonism and neutral antagonism at cannabinoid CB1 receptors. Life Sci 76:1307–1324PubMedGoogle Scholar
  93. Pitler TA, Alger BE (1992) Postsynaptic spike firing reduces synaptic GABAA responses in hippocampal pyramidal cells. J Neurosci 12:4122–4132PubMedGoogle Scholar
  94. Reich CG, Karson MA, Karnup SV et al. (2005) Regulation of IPSP theta rhythms by muscarinic receptors and endocannabinoids in hippocampus. J Neurophysiol 94:4290–4299PubMedGoogle Scholar
  95. Robbe D, Kopf M, Remaury A et al. (2002) Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc Natl Acad Sci USA 99:8384–8388PubMedGoogle Scholar
  96. Robbe D, Montgomery SM, Thome A et al. (2006) Cannabinoids reveal importance of spike timing coordination in hippocampal function. Nat Neurosci 9:1526–1533PubMedGoogle Scholar
  97. Ronesi J, Gerdeman GL, Lovinger DM (2004) Disruption of endocannabinoid release and striatal long-term depression by postsynaptic blockade of endocannabinoid membrane transport. J Neurosci 24:1673–1679PubMedGoogle Scholar
  98. Ryberg E, Larsson N, Sjogren S et al. (2007) The orphan receptor GPR55 is a novel cannabinoid receptor. Br J Pharmacol 152:1092–1101PubMedGoogle Scholar
  99. Safo PK, Regehr WG (2005) Endocannabinoids control the induction of cerebellar LTD. Neuron 48:647–659PubMedGoogle Scholar
  100. Shin JH, Linden DJ (2005) An NMDA receptor/nitric oxide cascade is involved in cerebellar LTD but is not localized to the parallel fiber terminal. J Neurophysiol 94:4281–4289PubMedGoogle Scholar
  101. Singla S, Kreitzer AC, Malenka RC (2007) Mechanisms for synapse specificity during striatal long-term depression. J Neurosci 27:5260–5264PubMedGoogle Scholar
  102. Sjostrom PJ, Turrigiano GG, Nelson SB (2003) Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron 39:641–654PubMedGoogle Scholar
  103. Sjostrom PJ, Turrigiano GG, Nelson SB (2004) Endocannabinoid-dependent neocortical layer-5 LTD in the absence of postsynaptic spiking. J Neurophysiol 92:3338–3343PubMedGoogle Scholar
  104. Starowicz K, Nigam S, Di Marzo V (2007) Biochemistry and pharmacology of endovanilloids. Pharmacol Ther 114:13–33PubMedGoogle Scholar
  105. Szabadits E, Cserep C, Ludanyi A et al. (2007) Hippocampal GABAergic synapses possess the molecular machinery for retrograde nitric oxide signaling. J Neurosci 27:8101–8111PubMedGoogle Scholar
  106. Takahashi KA, Linden DJ (2000) Cannabinoid receptor modulation of synapses received by cerebellar Purkinje cells. J Neurophysiol 83:1167–1180PubMedGoogle Scholar
  107. Trettel J, Levine ES (2002) Cannabinoids depress inhibitory synaptic inputs received by layer 2/3 pyramidal neurons of the neocortex. J Neurophysiol 88:534–539PubMedGoogle Scholar
  108. Tzounopoulos T, Rubio ME, Keen JE et al. (2007) Coactivation of pre- and postsynaptic signaling mechanisms determines cell-specific spike-timing-dependent plasticity. Neuron 54:291–301PubMedGoogle Scholar
  109. van Beugen BJ, Nagaraja RY, Hansel C (2006) Climbing fiber-evoked endocannabinoid signaling heterosynaptically suppresses presynaptic cerebellar long-term potentiation. J Neurosci 26:8289–8294PubMedGoogle Scholar
  110. Varma N, Carlson GC, Ledent C et al. (2001) Metabotropic glutamate receptors drive the endocannabinoid system in hippocampus. J Neurosci 21(RC188):1–5Google Scholar
  111. Varma N, Brager DH, Morishita W et al. (2002) Presynaptic factors in the regulation of DSI expression in hippocampus. Neuropharmacology 43:550–562PubMedGoogle Scholar
  112. Vasquez C, Lewis DL (1999) The CB1 cannabinoid receptor can sequester G-proteins, making them unavailable to couple to other receptors. J Neurosci 19:9271–9280PubMedGoogle Scholar
  113. Wagner JJ, Alger BE (1996) Increased neuronal excitability during depolarization-induced suppression of inhibition in rat hippocampus. J Physiol (Lond) 495:107–112Google Scholar
  114. Wang J, Zucker RS (2001) Photolysis-induced suppression of inhibition in rat hippocampal CA1 pyramidal neurons. J Physiol (Lond) 533:757–763Google Scholar
  115. Wilson RI, Nicoll RA (2001) Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410:588–592PubMedGoogle Scholar
  116. Wilson RI, Kunos G, Nicoll RA (2001) Presynaptic specificity of endocannabinoid signaling in the hippocampus. Neuron 31:453–462PubMedGoogle Scholar
  117. Yamasaki M, Hashimoto K, Kano M (2006) Miniature synaptic events elicited by presynaptic Ca2+ rise are selectively suppressed by cannabinoid receptor activation in cerebellar Purkinje cells. J Neurosci 26:86–95PubMedGoogle Scholar
  118. Yasuda H, Huang Y, Tsumoto T (2008) Regulation of excitability and plasticity by endocannabinoids and PKA in developing hippocampus. Proc Natl Acad Sci USA 105:3106–3111PubMedGoogle Scholar
  119. Yin HH, Lovinger DM (2006) Frequency-specific and D2 receptor-mediated inhibition of glutamate release by retrograde endocannabinoid signaling. Proc Natl Acad Sci USA 103:8251–8256PubMedGoogle Scholar
  120. Yin HH, Davis MI, Ronesi JA et al. (2006) The role of protein synthesis in striatal long-term depression. J Neurosci 26:11811–11820PubMedGoogle Scholar
  121. Zhu PJ, Lovinger DM (2005) Retrograde endocannabinoid signaling in a postsynaptic neuron/synaptic bouton preparation from basolateral amygdala. J Neurosci 25:6199–6207PubMedGoogle Scholar
  122. Zhu PJ, Lovinger DM (2007) Persistent synaptic activity produces long-lasting enhancement of endocannabinoid modulation and alters long-term synaptic plasticity. J Neurophysiol 97:4386–4389PubMedGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2009

Authors and Affiliations

  1. 1.Departments of Physiology and PsychiatryUniversity of Maryland School of MedicineBaltimoreUSA

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