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Cannabinoids pp 327–365Cite as

Effects of Cannabinoids on Neurotransmission

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Part of the book series: Handbook of Experimental Pharmacology ((HEP,volume 168))

Abstract

The CB1 cannabinoid receptor is widely distributed in the central and peripheral nervous system. Within the neuron, the CB1 receptor is often localised in axon terminals, and its activation leads to inhibition of transmitter release. The consequence is inhibition of neurotransmission via a presynaptic mechanism. Inhibition of glutamatergic, GABAergic, glycinergic, cholinergic, noradrenergic and serotonergic neurotransmission has been observed in many regions of the central nervous system. In the peripheral nervous system, CB1 receptor-mediated inhibition of adrenergic, cholinergic and sensory neuroeffector transmission has been frequently observed. It is characteristic for the ubiquitous operation of CB1 receptor-mediated presynaptic inhibition that antagonistic components of functional systems (for example, the excitatory and inhibitory inputs of the same neuron) are simultaneously inhibited by cannabinoids. Inhibition of voltage-dependent calcium channels, activation of potassium channels and direct interference with the synaptic vesicle release mechanism are all implicated in the cannabinoid-evoked inhibition of transmitter release. Many presynaptic CB1 receptors are subject to an endogenous tone, i.e. they are constitutively active and/or are continuously activated by endocannabinoids. Compared with the abundant data on presynaptic inhibition by cannabinoids, there are only a few examples for cannabinoid action on the somadendritic parts of neurons in situ.

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References

  • Acquas E, Pisanu A, Marrocu P, Di Chiara G (2000) Cannabinoid CB1 receptor agonists increase rat cortical and hippocampal acetylcholine release in vivo. Eur J Pharmacol 401:179–185

    Article  PubMed  CAS  Google Scholar 

  • Acquas E, Pisanu A, Marrocu P, Goldberg SR, Di Chiara G (2001) Δ 9-Tetrahydrocannabinol enhances cortical and hippocampal acetylcholine release in vivo: a microdialysis study. Eur J Pharmacol 419:155–161

    Article  PubMed  CAS  Google Scholar 

  • Ahluwalia J, Urban L, Bevan S, Nagy I (2003) Anandamide regulates neuropeptide release from capsaicin-sensitive primary sensory neurons by activating both the cannabinoid 1 receptor and the vanilloid receptor 1 in vitro. Eur J Neurosci 17:2611–2618

    Article  PubMed  Google Scholar 

  • Akinshola BE, Taylor RE, Ogunseitan AB, Onaivi ES (1999) Anandamide inhibition of recombinant AMPA receptor subunits in Xenopus oocytes is increased by forskolin and 8-bromo-cyclic AMP. Naunyn-Schmiedeberg’s Arch Pharmacol 360:242–248

    Article  CAS  Google Scholar 

  • Al-Hayani A, Davies SN (2000) Cannabinoid receptor mediated inhibition of excitatory synaptic transmission in the rat hippocampal slice is developmentally regulated. Br J Pharmacol 131:663–665

    Article  PubMed  CAS  Google Scholar 

  • Ameri A, Simmet T (2000) Effects of 2-arachidonoylglycerol, an endogenous cannabinoid, on neuronal activity in rat hippocampal slices. Naunyn-Schmiedeberg’s Arch Pharmacol 361:265–272

    Article  CAS  Google Scholar 

  • Ameri A, Wilhelm A, Simmet T (1999) Effects of the endogenous cannabinoid, anandamide, on neuronal activity in rat hippocampus slices. Br J Pharmacol 126:1831–1839

    Article  PubMed  CAS  Google Scholar 

  • Auclair N, Otani S, Soubrie P, Crepel F (2000) Cannabinoids modulate synaptic strength and plasticity at glutamatergic synapses of rat prefrontal cortex pyramidal neurons. J Neurophysiol 83:3287–3293

    PubMed  CAS  Google Scholar 

  • Azad SC, Eder M, Marsicano G, Lutz B, Zieglgänsberger W, Rammes G (2003) Activation of the cannabinoid receptor type 1 decreases glutamatergic and GABAergic synaptic transmission in the lateral amygdala of the mouse. Learn Mem 10:116–128

    Article  PubMed  Google Scholar 

  • Barann M, Molderings G, Brüss M, Bönisch H, Urban BW, Göthert M (2002) Direct inhibition by cannabinoids of human 5-HT3A receptors: probable involvement of an allosteric modulatory site. Br J Pharmacol 137:589–596

    Article  PubMed  CAS  Google Scholar 

  • Begg M, Dale N, Llaudet E, Molleman A, Parsons ME (2002) Modulation of the release of endogenous adenosine by cannabinoids in the myenteric plexus-longitudinal muscle preparation of the guinea-pig ileum. Br J Pharmacol 137:1298–1304

    Article  PubMed  CAS  Google Scholar 

  • Brown SP, Brenowitz SD, Regehr WG (2003a) Brief presynaptic bursts evoke synapse-specific retrograde inhibition mediated by endogenous cannabinoids. Nat Neurosci 6:1048–1057

    Article  PubMed  CAS  Google Scholar 

  • Brown TM, Brotchie JM, Fitzjohn SM (2003b) Cannabinoids decrease corticostriatal synaptic transmission via an effect on glutamate uptake. J Neurosci 23:11073–11077

    PubMed  CAS  Google Scholar 

  • Cadogan A-K, Alexander SPH, Boyd AE, Kendall DA (1997) Influence of cannabinoids on electrically evoked dopamine release and cyclic AMP generation in the rat striatum. J Neurochem 69:1131–1137

    PubMed  CAS  Google Scholar 

  • Carta G, Nava F, Gessa GL (1998) Inhibition of hippocampal acetylcholine release after acute and repeated Δ9-tetrahydrocannabinol in rats. Brain Res 809:1–4

    Article  PubMed  CAS  Google Scholar 

  • Caulfield MP, Brown DA (1992) Cannabinoid receptor agonists inhibit Ca current in NG108-15 neuroblastoma cells via a pertussis toxin-sensitive mechanism. Br J Pharmacol 106:231–232

    PubMed  CAS  Google Scholar 

  • Chan PKY, Yung W-H (1998) Occlusion of the presynaptic action of cannabinoids in rat substantia nigra pars reticulata by cadmium. Neurosci Lett 249:57–60

    Article  PubMed  CAS  Google Scholar 

  • Chan PKY, Chan SCY, Yung W-H (1998) Presynaptic inhibition of GABAergic inputs to rat substantia nigra pars reticulata neurones by a cannabinoid agonist. Neuroreport 9:671–675

    PubMed  CAS  Google Scholar 

  • Chemin J, Monteil A, Perez-Reyes E, Nargeot J, Lory P (2001) Direct inhibition of T-type calcium channels by the endogenous cannabinoid anandamide. EMBO J 20:7033–7040

    Article  PubMed  CAS  Google Scholar 

  • Christopoulos A, Coles P, Lay L, Lew MJ, Angus JA (2001) Pharmacological analysis of cannabinoid receptor activity in the rat vas deferens. Br J Pharmacol 132:1281–1291

    Article  PubMed  CAS  Google Scholar 

  • Compton DR, Harris LS, Lichtman AH Martin BR (1996) Marihuana. Pharmacological aspects of drug dependence. In: Schuster CR, KuharM J (eds) Handbook of Experimental Pharmacology. Springer, Heidelberg, pp 83–158

    Google Scholar 

  • Coutts AA, Pertwee RG (1997) Inhibition by cannabinoid receptor agonists of acetylcholine release from the guinea-pig myenteric plexus. Br J Pharmacol 121:1557–1566

    PubMed  CAS  Google Scholar 

  • Croci T, Manara L, Aureggi G, Guagnini F, Rinaldi-Carmona M, Maffrand J-P, Le Fur G, Mukenge S, Ferla G (1998) In vitro functional evidence of neuronal cannabinoid CB1 receptors in human ileum. Br J Pharmacol 125:1393–1395

    Article  PubMed  CAS  Google Scholar 

  • Daniel H, Crepel F (2001) Control of Ca2+ influx by cannabinoid and metabotropic glutamate receptors in rat cerebellar cortex requires K+ channels. J Physiol (Lond) 537:793–800

    Article  PubMed  CAS  Google Scholar 

  • Deadwyler SA, Hampson RE, Mu J, Whyte A, Childers S (1995) Cannabinoids modulate voltage sensitive potassium A-current in hippocampal neurons via a cAMP-dependent process. J Pharmacol Exp Ther 273:734–743

    PubMed  CAS  Google Scholar 

  • Deutsch DG, Goligorsky MS, Schmid PC, Krebsbach RJ, Schmid HHO, Das SK, Dey SK, Arreaza G, Thorup C, Stefano G, Moore L (1997) Production and physiological actions of anandamide in the vasculature of the rat kidney. J Clin Invest 100:1538–1546

    Article  PubMed  CAS  Google Scholar 

  • Diana MA, Marty A (2003) Characterization of depolarization-induced suppression of inhibition using paired interneuron-Purkinje cell recordings. J Neurosci 23:5906–5918

    PubMed  CAS  Google Scholar 

  • Diana MA, Levenes C, Mackie K, Marty A (2002) Short-term retrograde inhibition of GABAergic synaptic currents in rat Purkinje cells is mediated by endogenous cannabinoids. J Neurosci 22:200–208

    PubMed  CAS  Google Scholar 

  • Ellington HC, Cotter MA, Cameron NE, Ross RA (2002) The effect of cannabinoids on capsaicin-evoked calcitonin gene-related peptide (CGRP) release from the isolated paw skin of diabetic and non-diabetic rats. Neuropharmacology 42:966–975

    Article  PubMed  CAS  Google Scholar 

  • Engler B, Szabo B (2003) Cannabinoids inhibit striatopallidal neurotransmission in mice. Naunyn-Schmiedeberg’s Arch Pharmacol 367:R85

    Google Scholar 

  • Engler B, Szabo B (2004) Characterization of the effects of cannabinoids on synaptic transmission between caudate-putamen and globus pallidus. Naunyn-Schmiedeberg’s Arch Pharmacol 369:R80

    Google Scholar 

  • Fan P (1995) Cannabinoid agonists inhibit the activation of 5-HT3 receptors in rat nodose ganglion neurons. J Neurophysiol 73:907–910

    PubMed  CAS  Google Scholar 

  • Ferraro L, Tomasini MC, Gessa GL, Bebe BW, Tanganelli S, Antonelli T (2001) The cannabinoid receptor agonist WIN 55, 212-2 regulates glutamate transmission in rat cerebral cortex: an in vivo and in vitro study. Cerebral Cortex 11:728–733

    Article  PubMed  CAS  Google Scholar 

  • Fränkel S (1903) Chemie und Pharmakologie des Haschisch. Naunyn-Schmiedeberg’s Arch Exp Pathol Pharmakol 49:266–284

    Google Scholar 

  • Freund TF, Katona I, Piomelli D (2003) Role of endogenous cannabinoids in synaptic signaling. Physiol Rev 83:1017–1066

    PubMed  CAS  Google Scholar 

  • Garcia DE, Brown S, Hille B, Mackie K (1998) Protein kinase C disrupts cannabinoid actions by phosphorylation of the CB1 cannabinoid receptor. J Neurosci 18:2834–2841

    PubMed  CAS  Google Scholar 

  • Gerdeman G, Lovinger DM (2001) CB1 cannabinoid receptor inhibits synaptic release of glutamate in rat dorsolateral striatum. J Neurophysiol 85:468–471

    PubMed  CAS  Google Scholar 

  • Gessa GL, Casu MA, Carta G, Mascia MS (1998) Cannabinoids decrease acetylcholine release in the medial-prefrontal cortex and hippocampus, reversal by SR 141716A. Eur J Pharmacol 355:119–124

    Article  PubMed  CAS  Google Scholar 

  • Gifford AN, Ashby Jr CR (1996) Electrically evoked acetylcholine release from hippocampal slices is inhibited by the cannabinoid receptor agonist, WIN 55212-2, and is potentiated by the cannabinoid antagonist, SR 141716A. J Pharmacol Exp Ther 277:1431–1436

    PubMed  CAS  Google Scholar 

  • Gifford AN, Samiian L, Gatley JS, Ashby Jr CR (1997a) Examination of the effect of the cannabinoid receptor agonist, CP 55,940, on electrically evoked transmitter release from rat brain slices. Eur J Pharmacol 324:187–192

    Article  PubMed  CAS  Google Scholar 

  • Gifford AN, Tang Y, Gatley SJ, Volkow ND, Lan R, Makriyannis A (1997b) Effect of the cannabinoid receptor SPECT agent, AM 281, on hippocampal acetylcholine release from rat brain slices. Neurosci Lett 238:84–86

    Article  PubMed  CAS  Google Scholar 

  • Gifford AN, Bruneus M, Gatley SJ, Volkow ND (2000) Cannabinoid receptor-mediated inhibition of acetylcholine release from hippocampal and cortical synaptosomes. Br J Pharmacol 131:645–650

    Article  PubMed  CAS  Google Scholar 

  • Glass M, Dragunow M, Faull RLM (2000) The pattern of neurodegeneration in Huntington’s disease: a comparative study of cannabinoid, dopamine, adenosine and GABAA receptor alterations in the humanbasal ganglia inHuntington’s disease. Neuroscience 97:505–519

    Article  PubMed  CAS  Google Scholar 

  • Göbel I, Trendelenburg AU, Cox SL, Meyer A, Starke K (2000) Electrically evoked release of [3H] noradrenaline from mouse cultured sympathetic neurons: release-modulating heteroreceptors. J Neurochem 75:2087–2094

    PubMed  Google Scholar 

  • Hájos N, Freund TF (2002) Pharmacological separation of cannabinoid sensitive receptors on hippocampal excitatory and inhibitory fibers. Neuropharmacology 43:503–510

    PubMed  Google Scholar 

  • Hájos N, Katona I, Naiem SS, Mackie K, Ledent C, Mody I, Freund TF (2000) Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations. Eur J Neurosci 12:3239–3249

    PubMed  Google Scholar 

  • Hájos N, Ledent C, Freund TF (2001) Novel cannabinoid-sensitive receptor mediates inhibition of glutamatergic synaptic transmission in the hippocampus. Neuroscience 106:1–4

    PubMed  Google Scholar 

  • Hampson RE, Mu J, Deadwyler SA (2000) Cannabinoid and kappa opioid receptors reduce potassium K current via activation of Gs proteins in cultured hippocampal neurons. J Neurophysiol 84:2356–2364

    PubMed  CAS  Google Scholar 

  • Henry DJ, Chavkin C (1995) Activation of inwardly rectifying potassium channels (GIRK1) by co-expressed rat brain cannabinoid receptors in Xenopus oocytes. Neurosci Lett 186:91–94

    Article  PubMed  CAS  Google Scholar 

  • Herkenham M, Lynn AB, De Costa BR, Richfield EK (1991) Neuronal localization of cannabinoid receptors in the basal ganglia of the rat. Brain Res 547:267–274

    Article  PubMed  CAS  Google Scholar 

  • Himmi T, Perrin J, El Ouazzani T, Orsini J-C (1998) Neuronal responses to cannabinoid receptor ligands in the solitary tract nucleus. Eur J Pharmacol 359:49–54

    Article  PubMed  CAS  Google Scholar 

  • Hoffman AF, Lupica CR (2000) Mechanisms of cannabinoid inhibition of GABAA synaptic transmission in the hippocampus. J Neurosci 20:2470–2479

    PubMed  CAS  Google Scholar 

  • Hoffman AF, Lupica CR (2001) Direct actions of cannabinoids on synaptic transmission in the nucleus accumbens: a comparison with opioids. J Neurophysiol 85:72–83

    PubMed  CAS  Google Scholar 

  • Hoffman AF, Oz M, Caulder T, Lupica CR (2003a) Functional tolerance and blockade of long-term depression at synapses in the nucleus accumbens after chronic cannabinoid exposure. J Neurosci 23:4815–4820

    PubMed  CAS  Google Scholar 

  • Hoffman AF, Riegel AC, Lupica CR (2003b) Functional localization of cannabinoid receptors and endogenous cannabinoid production in distinct neuron populations of the hippocampus. Eur J Neurosci 18:524–534

    Article  PubMed  Google Scholar 

  • Huang C-C, Lo S-W, Hsu K-S (2001) Presynaptic mechanisms underlying cannabinoid inhibition of excitatory synaptic transmission in rat striatal neurons. J Physiol (Lond) 532:731–748

    PubMed  CAS  Google Scholar 

  • Huang C-C, Chen Y-L, Lo S-W, Hsu K-S (2002) Activation of cAMP-dependent protein kinase suppresses the presynaptic cannabinoid inhibition of glutamatergic transmission at corticostriatal synapses. Mol Pharmacol 61:578–585

    PubMed  CAS  Google Scholar 

  • Hurst DP, Lynch DL, Barnett-Norris J, Hyatt SM, Seltzman HH, Zhong M, Song ZH, Nie J, Lewis D, Reggio PH (2002) N-(Piperidin-1-yl)-5-(4-chlorophenyl)-1-(2,4-dichlorophenyl)-4-methyl-1H-pyrazole-3-carboxamide (SR141716A) interaction with LYS 3.28 (192) is crucial for its inverse agonism at the cannabinoid CB1 receptor. Mol Pharmacol 62:1274–1287

    Article  PubMed  CAS  Google Scholar 

  • Irving AJ, Coutts AA, Harvey J, Rae MG, Mackie K, Bewick GS, Pertwee RG (2000) Functional expression of cell surface cannabinoid CB1 receptors on presynaptic inhibitory terminals in cultured rat hippocampal neurons. Neuroscience 98:253–262

    Article  PubMed  CAS  Google Scholar 

  • Ishac EJN, Jiang L, Lake KD, Varga K, Abood ME, Kunos G (1996) Inhibition of exocytotic noradrenaline release by presynaptic cannabinoid CB1 receptors on peripheral sympathetic nerves. Br J Pharmacol 118:2023–2028

    PubMed  CAS  Google Scholar 

  • Izzo AA, Mascolo N, Borrelli F, Capasso F (1998) Excitatory transmission to the circular muscle of the guinea-pig ileum: evidence for the involvement of cannabinoid CB1 receptors. Br J Pharmacol 124:1363–1368

    PubMed  CAS  Google Scholar 

  • Jennings EA, Vaughan CW, Christie MJ (2001) Cannabinoid actions on rat superficial medullary dorsal horn neurons in vitro. J Physiol 534:805–812

    Article  PubMed  CAS  Google Scholar 

  • Kathmann M, Bauer U, Schlicker E, Göthert M (1999) Cannabinoid CB1 receptor-mediated inhibition of NMDA-and kainate-stimulated noradrenaline and dopamine release in the brain. Naunyn-Schmiedeberg’s Arch Pharmacol 359:466–470

    Article  CAS  Google Scholar 

  • Kathmann M, Weber B, Schlicker E (2001a) Cannabinoid CB1 receptor-mediated inhibition of acetylcholine release in the brain of NMRI, CD-1 and C57BL/6 J mice. Naunyn-Schmiedeberg’s Arch Pharmacol 363:50–56

    Article  CAS  Google Scholar 

  • Kathmann M, Weber B, Zimmer A, Schlicker E (2001b) Enhanced acetylcholine release in the hippocampus of cannabinoid CB1 receptor-deficient mice. Br J Pharmacol 132:1169–1173

    Article  PubMed  CAS  Google Scholar 

  • Katona I, Sperlagh B, Sik A, Köfalvi A, Vizi ES, Mackie K, Freund TF (1999) Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 19:4544–4558

    PubMed  CAS  Google Scholar 

  • Katona I, Sperlagh B, Magloczky Z, Santha E, Köfalvi A, Czirjak S, Mackie K, Vizi ES, Freund TF (2000) GABAergic interneurons are the targets of cannabinoid actions in the human hippocampus. Neuroscience 100:797–804

    Article  PubMed  CAS  Google Scholar 

  • Katona I, Rancz EA, Acsady L, Ledent C, Mackie K, Hajos N, Freund TF (2001) Distribution of CB1 cannabinoid receptors in the amygdala and their role in the control of GABAergic transmission. J Neurosci 21:9506–9518

    PubMed  CAS  Google Scholar 

  • Kim DJ, Thayer SA (2000) Activation of CB1 cannabinoid receptors inhibits neurotransmitter release from identified synaptic sites in rat hippocampal cultures. Brain Res 852:398–405

    Article  PubMed  CAS  Google Scholar 

  • Köfalvi A, Vizi ES, Ledent C, Sperlagh B (2003) Cannabinoids inhibit the release of [3H]glutamate from rodent hippocampal synaptosomes via a novel CB1 receptor-independent action. Eur J Neurosci 18:1973–1978

    PubMed  Google Scholar 

  • Kolasiewicz W, Wolfarth S, Ossowska K (1988) The role of the ventromedial thalamic nucleus in the catalepsy evoked from the substantia nigra pars reticulata in rats. Neurosci Lett 90:219–223

    Article  PubMed  CAS  Google Scholar 

  • Kouznetsova M, Kelley B, Shen M, Thayer SA (2002) Desensitization of cannabinoi dmediated presynaptic inhibition of neurotransmission between rat hippocampal neurons in culture. Mol Pharmacol 61:477–485

    Article  PubMed  CAS  Google Scholar 

  • Kreitzer AC, Regehr WG (2001) Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29:717–727

    Article  PubMed  CAS  Google Scholar 

  • Kreitzer AC, Carter AG, Regehr WG (2002) Inhibition of interneuron firing extends the spread of endocannabinoid signaling in the cerebellum. Neuron 34:787–796

    Article  PubMed  CAS  Google Scholar 

  • Lay L, Angus JA, Wright CE (2000) Pharmacological characterisation of cannabinoid CB1 receptors in the rat and mouse. Eur J Pharmacol 391:151–161

    Article  PubMed  CAS  Google Scholar 

  • Levenes C, Daniel H, Soubrie P, Crepel F (1998) Cannabinoids decrease excitatory synaptic transmission and impair long-term depression in rat cerebellar Purkinje cells. J Physiol (Lond) 510:867–879

    Article  PubMed  CAS  Google Scholar 

  • Lever IJ, Malcangio M (2002) CB1 receptor antagonist SR141716A increases capsaicinevoked release of Substance P fromthe adult mouse spinal cord. Br J Pharmacol 135:21–24

    PubMed  CAS  Google Scholar 

  • Lopez-Redondo F, Lees GM, Pertwee RG (1997) Effects of cannabinoid receptor ligands on electrophysiological properties of myenteric neurones of the guinea-pig ileum. Br J Pharmacol 122:330–334

    PubMed  CAS  Google Scholar 

  • Mackie K, Hille B (1992) Cannabinoids inhibit N-type calcium channels in neuroblastomaglioma cells. Proc Natl Acad Sci USA 89:3825–3829

    PubMed  CAS  Google Scholar 

  • Mackie K, Devane WA, Hille B (1993) Anandamide, an endogenous cannabinoid, inhibits calcium currents as a partial agonist in N 18 neuroblastoma cells. Mol Pharmacol 44:498–503

    PubMed  CAS  Google Scholar 

  • Mackie K, Lai Y, Westenbroek R, Mitchell R (1995) Cannabinoids activate an inwardly rectifying potassium conductance and inhibit Q-type calcium currents in AtT20 cells transfected with rat brain cannabinoid receptor. J Neurosci 15:6552–6561

    PubMed  CAS  Google Scholar 

  • Maejima T, Hashimoto K, Yoshida T, Aiba A, Kano M (2001) Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabinoid receptors. Neuron 31:463–475

    Article  PubMed  CAS  Google Scholar 

  • Mailleux P, Vanderhaeghen J-J (1992) Distribution of neuronal cannabinoid receptor in the adult rat brain: a comparative receptor binding radioautography and in situ hybridization histochemistry. Neuroscience 48:655–668

    Article  PubMed  CAS  Google Scholar 

  • Maingret F, Patel AJ, Lazdunski M, Honore E (2001) The endocannabinoid anandamide is a direct and selective blocker of the background K+ channel TASK-1. EMBO J 20:47–54

    Article  PubMed  CAS  Google Scholar 

  • Malinowska B, Godlewski G, Bucher B, Schlicker, E (1997) Cannabinoid CB1 receptormediated inhibition of the neurogenic vasopressor response in the pithed rat. Naunyn-Schmiedeberg’s Arch Pharmacol 356:197–202

    Article  CAS  Google Scholar 

  • Malinowska B, Piszcz J, Koneczny B, Hryniewicz A, Schlicker E (2001) Modulation of the cardiac autonomic transmission of pithed rats by presynaptic opioid OP4 and cannabinoid CB1 receptors. Naunyn-Schmiedeberg’s Arch Pharmacol 364:233–241

    CAS  Google Scholar 

  • Malone DT, Taylor DA (1999) Modulation by fluoxetine of striatal dopamine release following Δ9-tetrahydrocannabinol: a microdialysis study in conscious rats. Br J Pharmacol 128:21–26

    Article  PubMed  CAS  Google Scholar 

  • Mang CF, Erbelding D, Kilbinger H (2001) Differential effects of anandamide on acetylcholine release in the guinea-pig ileum mediated via vanilloid and non-CB1 receptors. Br J Pharmacol 134:161–167

    Article  PubMed  CAS  Google Scholar 

  • Manzoni OJ, Bockaert J (2001) Cannabinoids inhibit GABAergic synaptic transmission in mice nucleus accumbens. Eur J Pharmacol 412:R3–R5

    Article  PubMed  CAS  Google Scholar 

  • Marsicano G, Wotjak CT, Azad SC, Bisogno T, Rammes G, Cascio MG, Hermann H, Tang J, Hofmann C, Zieglgänsberger W, Di Marzo V, Lutz B (2002) The endogenous cannabinoid system controls extinction of aversive memories. Nature 418:530–534

    Article  PubMed  CAS  Google Scholar 

  • Matsuda LA, Bonner TI, Lolait SJ (1993) Localization of cannabinoid receptor mRNA in rat brain. J Comp Neurol 327:535–550

    Article  PubMed  CAS  Google Scholar 

  • McAllister SD, Griffin G, Satin LS, Abood ME (1999) Cannabinoid receptors can activate and inhibit G protein-coupled inwardly rectifying potassium channels in a Xenopus oocyte expression system. J Pharmacol Exp Ther 291:618–626

    PubMed  CAS  Google Scholar 

  • Melis M, Pistis M, Perra S, Muntoni AL, Pillolla G, Gessa GL (2004) Endocannabinoids mediate presynaptic inhibition of glutamatergic transmission in rat ventral tegmental area dopamine neurons through activation of CB1 receptors. J Neurosci 24:53–62

    PubMed  CAS  Google Scholar 

  • Mishima K, Egashira N, Matsumoto Y, Iwasaki K, Fujiwara M (2002) Involvement of reduced acetylcholine release in Δ9-tetrahydrocannabinol-induced impairment of spatial memory in the 8-arm radial maze. Life Sci 72:397–407

    Article  PubMed  CAS  Google Scholar 

  • Misner DL, Sullivan JM (1999) Mechanism of cannabinoid effects on long-term potentiation and depression in hippocampal CA1 neurons. J Neurosci 19:6795–6805

    PubMed  CAS  Google Scholar 

  • Molderings GJ, Likungu J, Göthert M (1999) Presynaptic cannabinoid and imidazoline receptors in the human heart and their potential relationship. Naunyn-Schmiedeberg’s Arch Pharmacol 360:157–164

    CAS  Google Scholar 

  • Morisset V, Urban L (2001) Cannabinoid-induced presynaptic inhibition of glutam’ EPSCs in substantia gelatinosa neurons of the rat spinal cord. J Neurophysiol 86:40–48

    PubMed  CAS  Google Scholar 

  • Mu J, Zhuang S-Y, Hampson RE, Deadwyler SA (2000) Protein kinase-dependent phosphorylation and cannabinoid receptor modulation of potassium A current (IA) in cultured rat hippocampal neurons. Pflügers Arch 439:541–546

    Article  PubMed  CAS  Google Scholar 

  • Nakatsuka T, Chen H-X, Roper SN, Gu JG (2003) Cannabinoid receptor-1 activation suppresses inhibitory synaptic activity in human dentate gyrus. Neuropharmacology 45:116–121

    Article  PubMed  CAS  Google Scholar 

  • Nakazi M, Bauer M, Nickel T, Kathmann M, Schlicker E (2000) Inhibition of serotonin release in the mouse brain via presynaptic cannabinoid CB1 receptors. Naunyn-Schmiedeberg’s Arch Pharmacol 361:19–24

    CAS  Google Scholar 

  • Nemeth J, Helyes Z, Than M, Jakab B, Pinter E, Szolcsanyi J (2003) Concentration-dependent dual effect of anandamide on sensory neuropeptide release from isolated rat tracheae. Neurosci Lett 336:89–92

    Article  PubMed  CAS  Google Scholar 

  • Nicholson RA, Liao C, Zheng J, David LS, Coyne L, Errington AC, Singh G, Lees G (2003) Sodium channel inhibition by anandamide and synthetic cannabimimetics in brain. Brain Res 978:194–204

    Article  PubMed  CAS  Google Scholar 

  • Niederhoffer N, Szabo B (1999) Effect of the cannabinoid receptor agonist WIN55212-2 on sympathetic cardiovascular regulation. Br J Pharmacol 126:457–466

    PubMed  CAS  Google Scholar 

  • Niederhoffer N, Hansen HH, Fernandez-Ruiz JJ, Szabo B (2001) Effects of cannabinoids on adrenaline release from adrenal medullary cells. Br J Pharmacol 134:1319–1327

    Article  PubMed  CAS  Google Scholar 

  • Niederhoffer N, Schmid K, Szabo B (2003) The peripheral sympathetic nervous system is the major target of cannabinoids in eliciting cardiovascular depression. Naunyn-Schmiedeberg’s Arch Pharmacol 367:434–443

    Article  CAS  Google Scholar 

  • Nogueron IM, Porgilsson B, Schneider WE, Stucky CL, Hillard CJ (2001) Cannabinoid receptor agonists inhibit depolarization-induced calcium influx in cerebellar granule neurons. J Neurochem 79:371–381

    Article  PubMed  CAS  Google Scholar 

  • Ohno-Shosaku T, Maejima T, Kano M (2001) Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 29:729–738

    PubMed  CAS  Google Scholar 

  • Oz M, Ravindran A, Diaz-Ruiz O, Zhang L, Morales M (2003) The endogenous cannabinoid anandamide inhibits α7 nicotinic acetylcholine receptor-mediated responses in Xenopus oocytes. J Pharmacol Exp Ther 306:1003–1010

    Article  PubMed  CAS  Google Scholar 

  • Pan X, Ikeda SR, Lewis DL (1996) Rat brain cannabinoid receptor modulates N-type Ca2+ channels in a neuronal expression system. Mol Pharmacol 49:707–714

    PubMed  CAS  Google Scholar 

  • Patel S, Hillard CJ (2001) Cannabinoid CB1 receptor agonists produce cerebellar dysfunction in mice. J Pharmacol Exp Ther 297:629–637

    PubMed  CAS  Google Scholar 

  • Pertwee RG, Fernando SR (1996) Evidence for the presence of cannabinoid CB1 receptors in mouse urinary bladder. Br J Pharmacol 118:2053–2058

    PubMed  CAS  Google Scholar 

  • Pertwee RG, Stevenson LA, Elrick DB, Mechoulam R, Corbett AD (1992) Inhibitory effects of certain enantiomeric cannabinoids in the mouse vas deferens and themyenteric plexus preparation of guinea-pig small intestine. Br J Pharmacol 105:980–984

    PubMed  CAS  Google Scholar 

  • Pertwee RG, Fernando SR, Griffin G, Ryan W, Razdan RK, Compton DR, Martin BR (1996a) Agonist-antagonist characterization of 6’-cyanohex-2’-yne-Δ8-tetrahydrocannabinol in two isolated tissue preparations. Eur J Pharmacol 315:195–201

    Article  PubMed  Google Scholar 

  • Pertwee RG, Fernando SR, Nash JE, Coutts AA (1996b) Further evidence for the presence of cannabinoid CB1 receptors in guinea-pig small intestine. Br J Pharmacol 118:2199–2205

    PubMed  CAS  Google Scholar 

  • Pertwee RG, Ross RA, Craib S, Thomas A (2002) (-)-Cannabidiol antagonizes cannabinoid receptor agonists and noradrenaline in the mouse vas deferens. Eur J Pharmacol 456:99–106

    Article  PubMed  CAS  Google Scholar 

  • Ralevic V (2003) Cannabinoid modulation of peripheral autonomic and sensory neurotransmission. Eur J Pharmacol 472:1–21

    Article  PubMed  CAS  Google Scholar 

  • Ralevic V, Kendall DA (2001) Cannabinoid inhibition of capsaicin-sensitive sensory neurotransmission in the rat mesenteric arterial bed. Eur J Pharmacol 418:117–125

    Article  PubMed  CAS  Google Scholar 

  • Ralevic V, Kendall DA (2002) Cannabinoids inhibit pre-and postjunctionally sympathetic neurotransmission in rat mesenteric arteries. Eur J Pharmacol 444:171–181

    Article  PubMed  CAS  Google Scholar 

  • Richardson JD, Kilo S, Hargreaves KM (1998) Cannabinoids reduce hyperalgesia and inflammation via interaction with peripheral CB1 receptors. Pain 75:111–119

    Article  PubMed  CAS  Google Scholar 

  • Riegel AC, Williams JT, Lupica CR (2003) Cannabinoid receptor activation depresses GABAB mediated synaptic responses in dopamine neurons. In: 2003 Symposium on the cannabinoids. International Cannabinoid Research Society, Burlington, p 23

    Google Scholar 

  • Robbe D, Alonso G, Duchamp F, Bockaert J, Manzoni OJ (2001) Localization and mechanisms of action of cannabinoid receptors at the glutamatergic synapses of the mouse nucleus accumbens. J Neurosci 21:109–116

    PubMed  CAS  Google Scholar 

  • Rodriguez JJ, Mackie K, Pickel VM (2001) Ultrastructural localization of the CB1 cannabinoid receptor in µ-opioid receptor patches of the rat caudate putamen nucleus. J Neurosci 21:823–833

    PubMed  CAS  Google Scholar 

  • Rubovitch V, Gafni M, Sarne Y (2002) The cannabinoid agonist DALN positively modulates L-type voltage-dependent calcium-channels in N18TG2 neuroblastoma cells. Mol Brain Res 101:93–102

    Article  PubMed  CAS  Google Scholar 

  • Ruiu S, Pinna GA, Marchese G, Mussinu JM, Saba P, Tambaro S, Casti P, Vargiu R, Pani L (2003) Synthesis and characterization of NESS 0327: a novel putative antagonist of the CB1 cannabinoid receptor. J Pharmacol Exp Ther 306:363–370

    Article  PubMed  CAS  Google Scholar 

  • Sanudo-Pena MC, Tsou K, Walker JM (1999) Motor actions of cannabinoids in the basal ganglia output nuclei. Life Sci 65:703–713

    PubMed  CAS  Google Scholar 

  • Schlicker E, Kathmann M (2001) Modulation of transmitter release via presynaptic cannabinoid receptors. Trends Pharmacol Sci 22:565–572

    Article  PubMed  CAS  Google Scholar 

  • Schlicker E, Timm J, Göthert M (1996) Cannabinoid receptor-mediated inhibition of dopamine release in the retina. Naunyn-Schmiedeberg’s Arch Pharmacol 354:791–795

    CAS  Google Scholar 

  • Schlicker E, Timm J, Zentner J, Göthert M (1997) Cannabinoid CB1 receptor-mediated inhibition of noradrenaline release in the human and guinea-pig hippocampus. Naunyn-Schmiedeberg’s Arch Pharmacol 356:583–589

    CAS  Google Scholar 

  • Schlicker E, Liedtke S, Flau K, Kathmann M (2002) Further evidence that the cannabinoid receptor inhibiting noradrenaline release in the guinea-pig brain belongs to the CB1 subtype and is subject to an endogenous tone. Pharmacologist 44(Suppl 1):A112

    Google Scholar 

  • Schlicker E, Redmer A, Werner A, Kathmann M (2003) Lack of CB1 receptors increases noradrenaline release in vas deferens without affecting atrial noradrenaline release or cortical acetylcholine release. Br J Pharmacol 140:323–328

    Article  PubMed  CAS  Google Scholar 

  • Schultheiß T, Flau K, Redmer A, Kathmann M, Reggio PH, Seltzman HH, Schlicker E (2004) The facilitatory effect of SR141716 on transmitter release in guinea-pig hippocampus is due to its inverse agonist activity at cannabinoid CB1 receptors. Naunyn-Schmiedeberg’s Arch Pharmacol 369(Suppl 1):R84

    Google Scholar 

  • Schweitzer P (2000) Cannabinoids decrease the K+ M-current in hippocampal CA1 neurons. J Neurosci 20:51–58

    PubMed  CAS  Google Scholar 

  • Seifert R, Wenzel-Seifert K (2002) Constitutive activity of G-protein-coupled receptors: cause of disease and common property of wild-type receptors. Naunyn-Schmiedeberg’s Arch Pharmacol 366:381–416

    Article  CAS  Google Scholar 

  • Shen M, Thayer SA (1999) Δ9-Tetrahydrocannabinol acts as a partial agonist to modulate glutamatergic synaptic transmission between rat hippocampal neurons in culture. Mol Pharmacol 55:8–13

    PubMed  CAS  Google Scholar 

  • Shen M, Piser TM, Seybold VS, Thayer SA (1996) Cannabinoid receptor agonists inhibit glutamatergic synaptic transmission in rat hippocampal cultures. J Neurosci 16:4322–4334

    PubMed  CAS  Google Scholar 

  • Starke K, Göthert M, Kilbinger H (1989) Modulation of neurotransmitter release by presynaptic autoreceptors. Physiol Rev 69:864–989

    PubMed  CAS  Google Scholar 

  • Steffens M, Szabo B, Klar M, Rominger A, Zentner J, Feuerstein TJ (2003) Modulation of electrically evoked acetylcholine release through cannabinoid CB1 receptors: evidence for an endocannabinoid tone in the human neocortex. Neuroscience 120:456–465

    Article  CAS  Google Scholar 

  • Storr M, Sibaev A, Marsicano G, Lutz B, Schusdziarra V, Timmermans JP, Allescher HD (2004) Cannabinoid receptor type 1 modulates excitatory and inhibitory neurotransmission in mouse colon. Am J Physiol Gastrointest Liver Physiol 286:G110–G117

    PubMed  CAS  Google Scholar 

  • Straiker A, Sullivan JM (2003) Cannabinoid receptor activation differentially modulates ion channels in photoreceptors of the tiger salamander. J Neurophysiol 89:2647–2654

    PubMed  CAS  Google Scholar 

  • Straiker AJ, Borden CR, Sullivan JM (2002) G-protein alpha subunit isoforms couple differentially to receptors that mediate presynaptic inhibition at rat hippocampal synapses. J Neurosci 22:2460–2468

    PubMed  CAS  Google Scholar 

  • Sullivan JM (1999) Mechanisms of cannabinoid-receptor-mediated inhibition of synaptic transmission in cultured hippocampal pyramidal neurons. J Neurophysiol 82:1286–1294

    PubMed  CAS  Google Scholar 

  • Szabo B, Dörner L, Pfreundtner C, Nörenberg W, Starke K (1998) Inhibition of GABAergic inhibitory postsynaptic currents by cannabinoids in rat corpus striatum. Neuroscience 85:395–403

    Article  PubMed  CAS  Google Scholar 

  • Szabo B, Müller T, Koch H (1999) Effects of cannabinoids on dopamine release in the corpus striatum and the nucleus accumbens in vitro. J Neurochem 73:1084–1089

    Article  PubMed  CAS  Google Scholar 

  • Szabo B, Wallmichrath I, Mathonia P, Pfreundtner C (2000) Cannabinoids inhibit excitatory neurotransmission in the substantia nigra pars reticulata. Neuroscience 97:89–97

    Article  PubMed  CAS  Google Scholar 

  • Szabo B, Nordheim U, Niederhoffer N (2001) Effects of cannabinoids on sympathetic and parasympathetic neuroeffector transmission in the rabbit heart. J Pharmacol Exp Ther 297:819–826

    PubMed  CAS  Google Scholar 

  • Szabo B, Siemes S, Wallmichrath I (2002) Inhibition of GABAergic neurotransmission in the ventral tegmental area by cannabinoids. Eur J Neurosci 15:2057–2061

    Article  PubMed  Google Scholar 

  • Szabo B, Than M, Wallmichrath I, Thorn D (2004) Analysis of the effects of cannabinoids on synaptic transmission between basket and Purkinje cells in the cerebellar cortex of the rat. J Pharmacol Exp Ther 310:915–925

    Article  PubMed  CAS  Google Scholar 

  • Takahashi KA, Linden DJ (2000) Cannabinoid receptor modulation of synapses received by cerebellar Purkinje cells. J Neurophysiol 83:1167–1180

    PubMed  CAS  Google Scholar 

  • Thompson SM, Capogna M, Scanziani M (1993) Presynaptic inhibition in the hippocampus. Trends Neurosci 16:222–227

    PubMed  CAS  Google Scholar 

  • Timm J, Marr I, Werthwein S, Elz S, Schunack W, Schlicker E (1998) H2 receptor-mediated facilitation and H3 receptor-mediated inhibition of noradrenaline release in the guinea-pig brain. Naunyn-Schmiedeberg’s Arch Pharmacol 357:232–239

    Article  CAS  Google Scholar 

  • Tognetto M, Amadesi S, Harrison S, Creminon C, Trevisani M, Carreras M, Matera M, Geppetti P, Bianchi A (2001) Anandamide excites central terminals of dorsal root ganglion neurons via vanilloid receptor-1 activation. J Neurosci 21:1104–1109

    PubMed  CAS  Google Scholar 

  • Trendelenburg AU, Cox SL, Schelb V, Klebroff W, Khairallah, Starke K (2000) Modulation of 3H-noradrenaline release by presynaptic opioid, cannabinoid and bradykinin receptors and β-adrenoceptors in mouse tissues. Br J Pharmacol 130:321–330

    Article  PubMed  CAS  Google Scholar 

  • Trettel J, Levine ES (2002) Cannabinoids depress inhibitory synaptic inputs received by layer 2/3 pyramidal neurons of the neocortex. J Neurophysiol 88:534–539

    PubMed  CAS  Google Scholar 

  • Trettel J, Levine ES (2003) Endocannabinoids mediate rapid retrograde signaling at interneuronμ pyramidal neuron synapses of the neocortex. J Neurophysiol 89:2334–2338

    PubMed  CAS  Google Scholar 

  • Tsou K, Brown S, Sanudo-Pena MC, Mackie K, Walker JM (1998) Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83:393–411

    PubMed  CAS  Google Scholar 

  • Turkanis SA, Partlow LM, Karler R (1991) Delta-9-tetrahydrocannabinol depresses inward sodium current in mouse neuroblastoma cells. Neuropharmacology 30:73–77

    Article  PubMed  CAS  Google Scholar 

  • Twitchell W, Brown S, Mackie K (1997) Cannabinoids inhibit N-and P/Q-type calcium channels in cultured rat hippocampal neurons. J Neurophysiol 78:43–50

    PubMed  CAS  Google Scholar 

  • Tzavara ET, Perry KW, Rodriguez DE, Bymaster F, Nomikos GG (2001) The cannabinoid CB1 receptor antagonist SR141716A increases norepinephrine outflow in the rat anterior hypothalamus. Eur J Pharmacol 426:R3–R4

    Article  PubMed  CAS  Google Scholar 

  • Tzavara ET, Davis RJ, Perry KW, Li X, Salhoff C, Witkin JM, Bymaster F, Nomikos GG (2003a) The CB1 receptor antagonist SR141716A selectively increases monoaminergic neurotransmission in the medial prefrontal cortex: implications for therapeutic actions. Br J Pharmacol 138:544–553

    Article  PubMed  CAS  Google Scholar 

  • Tzavara ET, Wade M, Nomikos GG (2003b) Biphasic effects of cannabinoids on acetylcholine release in the hippocampus: site and mechanism of action. J Neurosci 23:9374–9384

    PubMed  CAS  Google Scholar 

  • Van Vliet BJ, Nievelstein HNMW, Long SK, Kruse CG (2000) CB1 receptor-mediated effects on brain neurotransmitter systems. Eur Neuropsychopharmacol 10(Suppl 3):S182–S183

    Google Scholar 

  • Vaughan CW, McGregor IS, Christie McDJ (1999) Cannabinoid receptor activation inhibits GABAergic neurotransmission in rostral ventromedial medulla neurons in vitro. Br J Pharmacol 127:935–940

    Article  PubMed  CAS  Google Scholar 

  • Vaughan CW, Connor M, Bagley EE, Christie MJ (2000) Actions of cannabinoids on membrane properties and synaptic transmission in rat periaqueductal gray neurons in vitro. Mol Pharmacol 57:288–295

    PubMed  CAS  Google Scholar 

  • Verrico CD, Jentsch JD, Dazzi L, Roth RH (2003) Systemic, but not local, administration of cannabinoid CB1 receptor agonists modulate prefrontal cortical acetylcholine efflux in the rat. Synapse 48:178–183

    Article  PubMed  CAS  Google Scholar 

  • Vizi ES, Katona I, Freund TF (2001) Evidence for presynaptic cannabinoid CB1 receptor-mediated inhibition of noradrenaline release in the guinea pig lung. Eur J Pharmacol 431:237–244

    Article  PubMed  CAS  Google Scholar 

  • Wallmichrath I, Szabo B (2002a) Analysis of the effect of cannabinoids on GABAergic neurotransmission in the substantia nigra pars reticulata. Naunyn-Schmiedeberg’s Arch Pharmacol 365:326–334

    Article  CAS  Google Scholar 

  • Wallmichrath I, Szabo B (2002b) Cannabinoids inhibit striatonigral GABAergic neurotransmission in the mouse. Neuroscience 113:671–682

    Article  PubMed  CAS  Google Scholar 

  • Wallmichrath I, Szabo B (2003) Effects of cannabinoids on the glutamatergic neurotransmission between nucleus subthalamicus and globus pallidus. Naunyn-Schmiedeberg’s Arch Pharmacol 367:R83

    Google Scholar 

  • Wang S-J (2003) Cannabinoid CB1 receptor-mediated inhibition of glutamate release from rat hippocampal synaptosomes. Eur J Pharmacol 469:47–55

    Article  PubMed  CAS  Google Scholar 

  • Wilson RI, Nicoll RA (2001) Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410:588–592

    Article  PubMed  CAS  Google Scholar 

  • Wilson RI, Nicoll RA (2002) Endocannabinoid signaling in the brain. Science 296:678–682

    Article  PubMed  CAS  Google Scholar 

  • Wu L-G, Saggau P (1997) Presynaptic inhibition of elicited neurotransmitter release. Trends Neurosci 20:204–212

    Article  PubMed  CAS  Google Scholar 

  • Yoshida T, Hashimoto K, Zimmer A, Maejima T, Araishi K, Kano M (2002) The cannabinoid CB1 receptor mediates retrograde signals for depolarization-induced suppression of inhibition in cerebellar Purkinje cells. J Neurosci 22:1690–1697

    PubMed  CAS  Google Scholar 

  • Zimmer A, Zimmer AM, Hohmann AG, Herkenham M, Bonner TI (1999) Increased mortality, hypoactivity, and hypoalgesia in cannabinoid CB1 receptor knockout mice. Proc Natl Acad Sci USA 96:5780–5785

    Article  PubMed  CAS  Google Scholar 

  • Zygmunt PM, Petersson J, Andersson DA, Chuang H, Sorgard M, Di Marzo V, Julius D, Högestätt ED (1999) Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400:452–457

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Institut für Experimentelle und Klinische Pharmakologie und Toxikologie, Albert-Ludwigs-Universität, Albertstrasse 25, 79104, Freiburg, Germany

    B. Szabo

  2. Institut für Pharmakologie und Toxikologie, Rheinische Friedrich-Wilhelms-Universität, Reuterstrasse 2b, 53113, Bonn, Germany

    E. Schlicker

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  1. B. Szabo
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  1. School of Medical Sciences, Institute of Medical Science, University of Aberdeen, Foresterhill, Aberdeen, AB25 2ZD, Scotland, UK

    Roger G. Pertwee

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Szabo, B., Schlicker, E. (2005). Effects of Cannabinoids on Neurotransmission. In: Pertwee, R.G. (eds) Cannabinoids. Handbook of Experimental Pharmacology, vol 168. Springer, Berlin, Heidelberg. https://doi.org/10.1007/3-540-26573-2_11

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