Abstract
The striatum plays a critical role in mediating the goal-directed and habitual behaviors involved in the development of drug abuse and addiction. Cannabinoid receptor-dependent synaptic plasticity is a prominent regulator of striatal circuit function. It is increasingly clear that striatal endocannabinoid signaling impacts the development of drug abuse. The expression of endocannabinoid-mediated plasticity in the striatum is affected by disparate types of drugs of abuse, such as opiates and alcohol. Understanding the mechanism of endocannabinoid-mediated plasticity and its effects on striatal circuit function may elucidate how endocannabinoids shape addiction-related behavior and perhaps offer new therapeutic avenues for treating drug abuse.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Ade KK, Lovinger DM (2007) Anandamide regulates postnatal development of long-term synaptic plasticity in the rat dorsolateral striatum. J Neurosci 27:2403–2409
Adermark L (2011) Modulation of endocannabinoid-mediated long-lasting disinhibition of striatal output by cholinergic interneurons. Neuropharmacology 61:1314–1320
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 27:6781–6787
Adermark L, Lovinger DM (2007b) Retrograde endocannabinoid signaling at striatal synapses requires a regulated postsynaptic release step. Proc Natl Acad Sci U S A 104:20564–20569
Adermark L, Lovinger DM (2009) Frequency-dependent inversion of net striatal output by endocannabinoid-dependent plasticity at different synaptic inputs. J Neurosci 29:1375–1380
Adermark L, Talani G, Lovinger DM (2009) Endocannabinoid-dependent plasticity at GABAergic and glutamatergic synapses in the striatum is regulated by synaptic activity. Eur J Neurosci 29:32–41
Adermark L, Jonsson S, Ericson M, Soderpalm B (2011) Intermittent ethanol consumption depresses endocannabinoid-signaling in the dorsolateral striatum of rat. Neuropharmacology 61:1160–1165
Alger BE (2002) Retrograde signaling in the regulation of synaptic transmission: focus on endocannabinoids. Prog Neurobiol 68:247–286
Alvarez-Jaimes L, Polis I, Parsons LH (2008) Attenuation of cue-induced heroin-seeking behavior by cannabinoid CB1 antagonist infusions into the nucleus accumbens core and prefrontal cortex, but not basolateral amygdala. Neuropsychopharmacology 33(10):2483–2493
Ambrose LM, Unterwald EM, Van Bockstaele EJ (2004) Ultrastructural evidence for co-localization of dopamine D2 and micro-opioid receptors in the rat dorsolateral striatum. Anat Rec A Discov Mol Cell Evol Biol 279:583–591
Atwood BK, Mackie K (2010) CB2: a cannabinoid receptor with an identity crisis. Br J Pharmacol 160:467–479
Atwood BK, Kupferschmidt DA, Lovinger DM (2014a) Opioids induce dissociable forms of long-term depression of excitatory inputs to the dorsal striatum. Nat Neurosci 17:540–548
Atwood BK, Lovinger DM, Mathur BN (2014b) Presynaptic long-term depression mediated by G-coupled receptors. Trends Neurosci 37(11):663–673
Azad SC, Marsicano G, Eberlein I, Putzke J, Zieglgansberger W, Spanagel R, Lutz B (2001) Differential role of the nitric oxide pathway on delta(9)-THC-induced central nervous system effects in the mouse. Eur J Neurosci 13:561–568
Bagetta V, Picconi B, Marinucci S, Sgobio C, Pendolino V, Ghiglieri V, Fusco FR, Giampa C, Calabresi P (2011) Dopamine-dependent long-term depression is expressed in striatal spiny neurons of both direct and indirect pathways: implications for Parkinson’s disease. J Neurosci 31:12513–12522
Bamford NS, Robinson S, Palmiter RD, Joyce JA, Moore C, Meshul CK (2004a) Dopamine modulates release from corticostriatal terminals. J Neurosci 24:9541–9552
Bamford NS, Zhang H, Schmitz Y, Wu NP, Cepeda C, Levine MS, Schmauss C, Zakharenko SS, Zablow L, Sulzer D (2004b) Heterosynaptic dopamine neurotransmission selects sets of corticostriatal terminals. Neuron 42:653–663
Beltramo M, Stella N, Calignano A, Lin SY, Makriyannis A, Piomelli D (1997) Functional role of high-affinity anandamide transport, as revealed by selective inhibition. Science 277:1094–1097
Bennett BD, Wilson CJ (1999) Spontaneous activity of neostriatal cholinergic interneurons in vitro. J Neurosci 19:5586–5596
Berretta S, Parthasarathy HB, Graybiel AM (1997) Local release of GABAergic inhibition in the motor cortex induces immediate-early gene expression in indirect pathway neurons of the striatum. J Neurosci 17:4752–4763
Bisogno T, Howell F, Williams G, Minassi A, Cascio MG, Ligresti A, Matias I, Schiano-Moriello A, Paul P, Williams EJ, Gangadharan U, Hobbs C, Di Marzo V, Doherty P (2003) Cloning of the first sn1-DAG lipases points to the spatial and temporal regulation of endocannabinoid signaling in the brain. J Cell Biol 163:463–468
Bolam JP, Izzo PN, Graybiel AM (1988) Cellular substrate of the histochemically defined striosome/matrix system of the caudate nucleus: a combined Golgi and immunocytochemical study in cat and ferret. Neuroscience 24:853–875
Brown SJ, James S, Reddington M, Richardson PJ (1990) Both A1 and A2a purine receptors regulate striatal acetylcholine release. J Neurochem 55:31–38
Burattini C, Battistini G, Tamagnini F, Aicardi G (2014) Low-frequency stimulation evokes serotonin release in the nucleus accumbens and induces long-term depression via production of endocannabinoid. J Neurophysiol 111:1046–1055
Cadogan AK, Alexander SP, Boyd EA, Kendall DA (1997) Influence of cannabinoids on electrically evoked dopamine release and cyclic AMP generation in the rat striatum. J Neurochem 69:1131–1137
Caillé S, Parsons LH (2006) Cannabinoid modulation of opiate reinforcement through the ventral striatopallidal pathway. Neuropsychopharmacology 31(4):804–813
Calabresi P, Maj R, Mercuri NB, Bernardi G (1992a) Coactivation of D1 and D2 dopamine receptors is required for long-term synaptic depression in the striatum. Neurosci Lett 142:95–99
Calabresi P, Maj R, Pisani A, Mercuri NB, Bernardi G (1992b) Long-term synaptic depression in the striatum: physiological and pharmacological characterization. J Neurosci 12:4224–4233
Calabresi P, Mercuri NB, Sancesario G, Bernardi G (1993) Electrophysiology of dopamine-denervated striatal neurons. Implications for Parkinson’s disease. Brain 116(Pt 2):433–452
Calabresi P, Pisani A, Mercuri NB, Bernardi G (1994) Post-receptor mechanisms underlying striatal long-term depression. J Neurosci 14:4871–4881
Calabresi P, Saiardi A, Pisani A, Baik JH, Centonze D, Mercuri NB, Bernardi G, Borrelli E (1997) Abnormal synaptic plasticity in the striatum of mice lacking dopamine D2 receptors. J Neurosci 17:4536–4544
Calabresi P, Centonze D, Gubellini P, Marfia GA, Bernardi G (1999a) Glutamate-triggered events inducing corticostriatal long-term depression. J Neurosci 19:6102–6110
Calabresi P, Gubellini P, Centonze D, Sancesario G, Morello M, Giorgi M, Pisani A, Bernardi G (1999b) A critical role of the nitric oxide/cGMP pathway in corticostriatal long-term depression. J Neurosci 19:2489–2499
Canales JJ (2005) Stimulant-induced adaptations in neostriatal matrix and striosome systems: transiting from instrumental responding to habitual behavior in drug addiction. Neurobiol Learn Mem 83:93–103
Castelli MP, Paola Piras A, D’Agostino A, Pibiri F, Perra S, Gessa GL, Maccarrone M, Pistis M (2007) Dysregulation of the endogenous cannabinoid system in adult rats prenatally treated with the cannabinoid agonist WIN 55,212-2. Eur J Pharmacol 573:11–19
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
Ceccarini J, Kuepper R, Kemels D, van Os J, Henquet C, Van Laere K (2015) [18F]MK-9470 PET measurement of cannabinoid CB1 receptor availability in chronic cannabis users. Addict Biol 20(2):357–367
Centonze D, Grande C, Saulle E, Martin AB, Gubellini P, Pavon N, Pisani A, Bernardi G, Moratalla R, Calabresi P (2003a) Distinct roles of D1 and D5 dopamine receptors in motor activity and striatal synaptic plasticity. J Neurosci 23:8506–8512
Centonze D, Gubellini P, Pisani A, Bernardi G, Calabresi P (2003b) Dopamine, acetylcholine and nitric oxide systems interact to induce corticostriatal synaptic plasticity. Rev Neurosci 14:207–216
Centonze D, Battista N, Rossi S, Mercuri NB, Finazzi-Agro A, Bernardi G, Calabresi P, Maccarrone M (2004a) A critical interaction between dopamine D2 receptors and endocannabinoids mediates the effects of cocaine on striatal gabaergic Transmission. Neuropsychopharmacology 29:1488–1497
Centonze D, Gubellini P, Usiello A, Rossi S, Tscherter A, Bracci E, Erbs E, Tognazzi N, Bernardi G, Pisani A, Calabresi P, Borrelli E (2004b) Differential contribution of dopamine D2S and D2L receptors in the modulation of glutamate and GABA transmission in the striatum. Neuroscience 129:157–166
Cepeda C, Buchwald NA, Levine MS (1993) Neuromodulatory actions of dopamine in the neostriatum are dependent upon the excitatory amino acid receptor subtypes activated. Proc Natl Acad Sci U S A 90:9576–9580
Chen G, Cuzon Carlson VC, Wang J, Beck A, Heinz A, Ron D, Lovinger DM, Buck KJ (2011a) Striatal involvement in human alcoholism and alcohol consumption, and withdrawal in animal models. Alcohol Clin Exp Res 35(10):1739–1748
Chen M, Wan Y, Ade K, Ting J, Feng G, Calakos N (2011b) Sapap3 deletion anomalously activates short-term endocannabinoid-mediated synaptic plasticity. J Neurosci 31:9563–9573
Chepkova AN, Fleischer W, Kazmierczak T, Doreulee N, Haas HL, Sergeeva OA (2009) Developmental alterations of DHPG-induced long-term depression of corticostriatal synaptic transmission: switch from NMDA receptor-dependent towards CB1 receptor-dependent plasticity. Pflugers Arch 459:131–141
Choi S, Lovinger DM (1997a) Decreased frequency but not amplitude of quantal synaptic responses associated with expression of corticostriatal long-term depression. J Neurosci 17:8613–8620
Choi S, Lovinger DM (1997b) Decreased probability of neurotransmitter release underlies striatal long-term depression and postnatal development of corticostriatal synapses. Proc Natl Acad Sci U S A 94:2665–2670
Clarke RB, Adermark L (2010) Acute ethanol treatment prevents endocannabinoid-mediated long-lasting disinhibition of striatal output. Neuropharmacology 58:799–805
Cohen C, Perrault G, Voltz C, Steinberg R, Soubrié P (2002) SR141716, a central cannabinoid (CB(1)) receptor antagonist, blocks the motivational and dopamine-releasing effects of nicotine in rats. Behav Pharmacol 13(5–6):451–463
Concannon RM, Okine BN, Finn DP, Dowd E (2015) Differential upregulation of the cannabinoid CB(2) receptor in neurotoxic and inflammation-driven rat models of Parkinson’s disease. Exp Neurol 269:133–141
Corbille AG, Valjent E, Marsicano G, Ledent C, Lutz B, Herve D, Girault JA (2007) Role of cannabinoid type 1 receptors in locomotor activity and striatal signaling in response to psychostimulants. J Neurosci 27:6937–6947
Corbit LH, Nie H, Janak PH (2012) Habitual alcohol seeking: time course and the contribution of subregions of the dorsal striatum. Biol Psychiatry 72(5):389–395
Cravatt BF, Giang DK, Mayfield SP, Boger DL, Lerner RA, Gilula NB (1996) Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature 384:83–87
Cui Y, Paille V, Xu H, Genet S, Delord B, Fino E, Berry H, Venance L (2015) Endocannabinoids mediate bidirectional striatal spike-timing-dependent plasticity. J Physiol 593:2833–2849
Cuzon Carlson VC, Seabold GK, Helms CM, Garg N, Odagiri M, Rau AR, Daunais J, Alvarez VA, Lovinger DM, Grant KA (2011) Synaptic and morphological neuroadaptations in the putamen associated with long-term, relapsing alcohol drinking in primates. Neuropsychopharmacology 36(12):2513–2528
Davis MI, Puhl HL 3rd (2011) Nr4a1-eGFP is a marker of striosome-matrix architecture, development and activity in the extended striatum. PLoS One 6:e16619
Day TA, Rakhshan F, Deutsch DG, Barker EL (2001) Role of fatty acid amide hydrolase in the transport of the endogenous cannabinoid anandamide. Mol Pharmacol 59:1369–1375
De Luca MA, Valentini V, Bimpisidis Z, Cacciapaglia F, Caboni P, Di Chiara G (2014) Endocannabinoid 2-Arachidonoylglycerol self-administration by Sprague-Dawley rats and stimulation of in vivo Dopamine transmission in the nucleus accumbens shell. Front Psych 5:140
DePoy L, Daut R, Brigman JL, MacPherson K, Crowley N, Gunduz-Cinar O, Pickens CL, Cinar R, Saksida LM, Kunos G, Lovinger DM, Bussey TJ, Camp MC, Holmes A (2013) Chronic alcohol produces neuroadaptations to prime dorsal striatal learning. Proc Natl Acad Sci U S A 110:14783–14788
Desban M, Kemel ML, Glowinski J, Gauchy C (1993) Spatial organization of patch and matrix compartments in the rat striatum. Neuroscience 57:661–671
Deutsch DG, Glaser ST, Howell JM, Kunz JS, Puffenbarger RA, Hillard CJ, Abumrad N (2001) The cellular uptake of anandamide is coupled to its breakdown by fatty-acid amide hydrolase. J Biol Chem 276:6967–6973
Devane WA, Hanus L, Breuer A, Pertwee RG, Stevenson LA, Griffin G, Gibson D, Mandelbaum A, Etinger A, Mechoulam R (1992) Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258:1946–1949
Dhawan J, Deng H, Gatley SJ, Makriyannis A, Akinfeleye T, Bruneus M, Dimaio AA, Gifford AN (2006) Evaluation of the in vivo receptor occupancy for the behavioral effects of cannabinoids using a radiolabeled cannabinoid receptor agonist, R-[125/131I]AM2233. Synapse 60:93–101
Di Marzo V, Gianfrani C, De Petrocellis L, Milone A, Cimino G (1994) Polyunsaturated-fatty-acid oxidation in Hydra: regioselectivity, substrate-dependent enantioselectivity and possible biological role. Biochem J 300(Pt 2):501–507
Dinh TP, Carpenter D, Leslie FM, Freund TF, Katona I, Sensi SL, Kathuria S, Piomelli D (2002a) Brain monoglyceride lipase participating in endocannabinoid inactivation. Proc Natl Acad Sci U S A 99:10819–10824
Dinh TP, Freund TF, Piomelli D (2002b) A role for monoglyceride lipase in 2-arachidonoylglycerol inactivation. Chem Phys Lipids 121:149–158
Donoghue JP, Herkenham M (1986) Neostriatal projections from individual cortical fields conform to histochemically distinct striatal compartments in the rat. Brain Res 365:397–403
Doreulee N, Sergeeva OA, Yanovsky Y, Chepkova AN, Selbach O, Godecke A, Schrader J, Haas HL (2003) Cortico-striatal synaptic plasticity in endothelial nitric oxide synthase deficient mice. Brain Res 964:159–163
Dowie MJ, Grimsey NL, Hoffman T, Faull RL, Glass M (2014) Cannabinoid receptor CB2 is expressed on vascular cells, but not astroglial cells in the post-mortem human Huntington’s disease brain. J Chem Neuroanat 59-60:62–71
Eblen F, Graybiel AM (1995) Highly restricted origin of prefrontal cortical inputs to striosomes in the macaque monkey. J Neurosci 15:5999–6013
Ebrahimi A, Pochet R, Roger M (1992) Topographical organization of the projections from physiologically identified areas of the motor cortex to the striatum in the rat. Neurosci Res 14:39–60
Egertova M, Elphick MR (2000) Localisation of cannabinoid receptors in the rat brain using antibodies to the intracellular C-terminal tail of CB. J Comp Neurol 422:159–171
Emson PC, Waldvogel HJ, Faull RLM (2010) Neurotransmitter receptors in the basal ganglia. In: Steiner H, Tseng KY (eds) Handbook of behavioral neuroscience. Handbook of basal ganglia structure and function, vol 20. pp 75–96
Everitt BJ, Robbins TW (2016) Drug addiction: Updating actions to habits to compulsions ten years on. Annu Rev Psychol 67:23–50
Fegley D, Kathuria S, Mercier R, Li C, Goutopoulos A, Makriyannis A, Piomelli D (2004a) Anandamide transport is independent of fatty-acid amide hydrolase activity and is blocked by the hydrolysis-resistant inhibitor AM1172. Proc Natl Acad Sci U S A 101:8756–8761
Ferre S, Fredholm BB, Morelli M, Popoli P, Fuxe K (1997) Adenosine-dopamine receptor-receptor interactions as an integrative mechanism in the basal ganglia. Trends Neurosci 20:482–487
Ferrer B, Bermudez-Silva FJ, Bilbao A, Alvarez-Jaimes L, Sanchez-Vera I, Giuffrida A, Serrano A, Baixeras E, Khaturia S, Navarro M, Parsons LH, Piomelli D, Rodriguez de Fonseca F (2007) Regulation of brain anandamide by acute administration of ethanol. Biochem J 404:97–104
Fino E, Glowinski J, Venance L (2005) Bidirectional activity-dependent plasticity at corticostriatal synapses. J Neurosci 25:11279–11287
Fino E, Paille V, Cui Y, Morera-Herreras T, Deniau JM, Venance L (2010) Distinct coincidence detectors govern the corticostriatal spike timing-dependent plasticity. J Physiol 588:3045–3062
Flores-Hernandez J, Galarraga E, Bargas J (1997) Dopamine selects glutamatergic inputs to neostriatal neurons. Synapse 25:185–195
Fourgeaud L, Mato S, Bouchet D, Hemar A, Worley PF, Manzoni OJ (2004) A single in vivo exposure to cocaine abolishes endocannabinoid-mediated long-term depression in the nucleus accumbens. J Neurosci 24:6939–6945
Freiman I, Anton A, Monyer H, Urbanski MJ, Szabo B (2006) Analysis of the effects of cannabinoids on identified synaptic connections in the caudate-putamen by paired recordings in transgenic mice. J Physiol 575:789–806
French ED, Dillon K, Wu X (1997) Cannabinoids excite dopamine neurons in the ventral tegmentum and substantia nigra. Neuroreport 8:649–652
Fusco FR, Martorana A, Giampa C, De March Z, Farini D, D’Angelo V, Sancesario G, Bernardi G (2004) Immunolocalization of CB1 receptor in rat striatal neurons: a confocal microscopy study. Synapse 53:159–167
Fuxe K, Marcellino D, Genedani S, Agnati L (2007) Adenosine A(2A) receptors, dopamine D(2) receptors and their interactions in Parkinson’s disease. Mov Disord 22:1990–2017
Gao Y, Vasilyev DV, Goncalves MB, Howell FV, Hobbs C, Reisenberg M, Shen R, Zhang MY, Strassle BW, Lu P, Mark L, Piesla MJ, Deng K, Kouranova EV, Ring RH, Whiteside GT, Bates B, Walsh FS, Williams G, Pangalos MN, Samad TA, Doherty P (2010) Loss of retrograde endocannabinoid signaling and reduced adult neurogenesis in diacylglycerol lipase knock-out mice. J Neurosci 30:2017–2024
Gardner EL (2002) Addictive potential of cannabinoids: the underlying neurobiology. Chem Phys Lipids 121:267–290
Gardner EL (2005) Endocannabinoid signaling system and brain reward: emphasis on dopamine. Pharmacol Biochem Behav 81:263–284
Gerdeman G, Lovinger DM (2001) CB1 cannabinoid receptor inhibits synaptic release of glutamate in rat dorsolateral striatum. J Neurophysiol 85:468–471
Gerdeman GL, Ronesi J, Lovinger DM (2002) Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat Neurosci 5:446–451
Gerfen CR (1992) The neostriatal mosaic: multiple levels of compartmental organization. Trends Neurosci 15:133–139
Gerfen CR, Bolam JP (2010) The neuroanatomical organization of the basal ganglia. In: Steiner H, Tseng K.Y (eds) Handbook of behavioral neuroscience. Handbook of basal ganglia structure and function, vol 20. pp 3–28
Giuffrida A, Parsons LH, Kerr TM, Rodriguez de Fonseca F, Navarro M, Piomelli D (1999) Dopamine activation of endogenous cannabinoid signaling in dorsal striatum. Nat Neurosci 2:358–363
Glass M, Brotchie JM, Maneuf YP (1997) Modulation of neurotransmission by cannabinoids in the basal ganglia. Eur J Neurosci 9:199–203
Gonsiorek W, Lunn C, Fan X, Narula S, Lundell D, Hipkin RW (2000) Endocannabinoid 2-arachidonyl glycerol is a full agonist through human type 2 cannabinoid receptor: antagonism by anandamide. Mol Pharmacol 57:1045–1050
Goodman J, Packard MG (2014) Peripheral and intra-dorsolateral striatum injections of the cannabinoid receptor agonist WIN 55,212-2 impair consolidation of stimulus-response memory. Neuroscience 274:128–137
Goodman J, Packard MG (2015) The influence of cannabinoids on learning and memory processes of the dorsal striatum. Neurobiol Learn Mem 125:1–14
Gough AL, Olley JE (1978) Catalepsy induced by intrastriatal injections of delta9-THC and 11-OH-delta9-THC in the rat. Neuropharmacology 17(2):137–144
Gremel CM, Costa RM (2013) Orbitofrontal and striatal circuits dynamically encode the shift between goal-directed and habitual actions. Nat Commun 4:2264
Gremel C, Chancey J, Atwood B, Luo G, Neve R, Ramakrishnan C, Deisseroth K, Lovinger D, Costa R (2016) Endocannabinoid modulation of orbitostriatal circuits gates habit formation. Neuron 90(6):1312–1324
Grueter BA, Brasnjo G, Malenka RC (2010) Postsynaptic TRPV1 triggers cell type-specific long-term depression in the nucleus accumbens. Nat Neurosci 13:1519–1525
Gubellini P, Saulle E, Centonze D, Bonsi P, Pisani A, Bernardi G, Conquet F, Calabresi P (2001) Selective involvement of mGlu1 receptors in corticostriatal LTD. Neuropharmacology 40:839–846
Gubellini P, Picconi B, Bari M, Battista N, Calabresi P, Centonze D, Bernardi G, Finazzi-Agro A, Maccarrone M (2002) Experimental parkinsonism alters endocannabinoid degradation: implications for striatal glutamatergic transmission. J Neurosci 22:6900–6907
Guegan T, Cutando L, Gangarossa G, Santini E, Fisone G, Martinez A, Valjent E, Maldonado R, Martin M (2013) Operant behavior to obtain palatable food modifies ERK activity in the brain reward circuit. Eur Neuropsychopharmacol 23(3):240–252
Gulyas AI, Cravatt BF, Bracey MH, Dinh TP, Piomelli D, Boscia F, Freund TF (2004) Segregation of two endocannabinoid-hydrolyzing enzymes into pre- and postsynaptic compartments in the rat hippocampus, cerebellum and amygdala. Eur J Neurosci 20:441–458
Hart CL (2005) Increasing treatment options for cannabis dependence: a review of potential pharmacotherapies. Drug Alcohol Depend 80:147–159
Hashimotodani Y, Ohno-Shosaku T, Tanimura A, Kita Y, Sano Y, Shimizu T, Di Marzo V, Kano M (2013) Acute inhibition of diacylglycerol lipase blocks endocannabinoid-mediated retrograde signalling: evidence for on-demand biosynthesis of 2-arachidonoylglycerol. J Physiol 591:4765–4776
Haughey HM, Marshall E, Schacht JP, Louis A, Hutchison KE (2008) Marijuana withdrawal and craving: influence of the cannabinoid receptor 1 (CNR1) and fatty acid amide hydrolase (FAAH) genes. Addiction 103(10):1678–1686
Heifets BD, Chevaleyre V, Castillo PE (2008) Interneuron activity controls endocannabinoid-mediated presynaptic plasticity through calcineurin. Proc Natl Acad Sci U S A 105:10250–10255
Henriksson BG, Järbe TUC (1972) Δ9-Tetrahydrocannabinol used as discriminative stimulus for rats in position learning in a T-shaped water maze. Psychon Sci 27:25–26
Herkenham M, Lynn AB, de Costa BR, Richfield EK (1991a) Neuronal localization of cannabinoid receptors in the basal ganglia of the rat. Brain Res 547:267–274
Herkenham M, Lynn AB, Johnson MR, Melvin LS, de Costa BR, Rice KC (1991b) Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J Neurosci 11:563–583
Hernandez G, Cheer JF (2012) Effect of CB1 receptor blockade on food-reinforced responding and associated nucleus accumbens neuronal activity in rats. J Neurosci 32(33):11467–11477
Hernandez M, Berrendero F, Suarez I, Garcia-Gil L, Cebeira M, Mackie K, Ramos JA, Fernandez-Ruiz J (2000) Cannabinoid CB(1) receptors colocalize with tyrosine hydroxylase in cultured fetal mesencephalic neurons and their activation increases the levels of this enzyme. Brain Res 857:56–65
Hernandez G, Oleson EB, Gentry RN, Abbas Z, Bernstein DL, Arvanitogiannis A, Cheer JF (2014) Endocannabinoids promote cocaine-induced impulsivity and its rapid dopaminergic correlates. Biol Psychiatry 75(6):487–498
Hernandez-Lopez S, Tkatch T, Perez-Garci E, Galarraga E, Bargas J, Hamm H, Surmeier DJ (2000) D2 dopamine receptors in striatal medium spiny neurons reduce L-type Ca2+ currents and excitability via a novel PLC[beta]1-IP3-calcineurin-signaling cascade. J Neurosci 20:8987–8995
Hilario MR, Clouse E, Yin HH, Costa RM (2007) Endocannabinoid signaling is critical for habit formation. Front Integr Neurosci 1:6
Hillard CJ, Jarrahian A (2000) The movement of N-arachidonoylethanolamine (anandamide) across cellular membranes. Chem Phys Lipids 108:123–134
Hillard CJ, Edgemond WS, Jarrahian A, Campbell WB (1997) Accumulation of N-arachidonoylethanolamine (anandamide) into cerebellar granule cells occurs via facilitated diffusion. J Neurochem 69:631–638
Hoffman AF, Oz M, Caulder T, Lupica CR (2003) Functional tolerance and blockade of long-term depression at synapses in the nucleus accumbens after chronic cannabinoid exposure. J Neurosci 23:4815–4820
Hohmann AG, Herkenham M (2000) Localization of cannabinoid CB(1) receptor mRNA in neuronal subpopulations of rat striatum: a double-label in situ hybridization study. Synapse 37:71–80
Howe AR, Surmeier DJ (1995) Muscarinic receptors modulate N-, P-, and L-type Ca2+ currents in rat striatal neurons through parallel pathways. J Neurosci 15:458–469
Howlett AC, Barth F, Bonner TI, Cabral G, Casellas P, Devane WA, Felder CC, Herkenham M, Mackie K, Martin BR, Mechoulam R, Pertwee RG (2002) International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol Rev 54:161–202
Hsu KS, Huang CC, Yang CH, Gean PW (1995) Presynaptic D2 dopaminergic receptors mediate inhibition of excitatory synaptic transmission in rat neostriatum. Brain Res 690:264–268
Hu SS, Mackie K (2015) Distribution of the Endocannabinoid system in the central nervous system. Handb Exp Pharmacol 231:59–93
Huang CC, Lo SW, Hsu KS (2001) Presynaptic mechanisms underlying cannabinoid inhibition of excitatory synaptic transmission in rat striatal neurons. J Physiol 532:731–748
Huang CC, Chen YL, Lo SW, Hsu KS (2002) Activation of cAMP-dependent protein kinase suppresses the presynaptic cannabinoid inhibition of glutamatergic transmission at corticostriatal synapses. Mol Pharmacol 61:578–585
Huang YC, Wang SJ, Chiou LC, Gean PW (2003) Mediation of amphetamine-induced long-term depression of synaptic transmission by CB1 cannabinoid receptors in the rat amygdala. J Neurosci 23:10311–10320
James S, Richardson PJ (1993) The subcellular distribution of [3H]-CGS 21680 binding sites in the rat striatum: copurification with cholinergic nerve terminals. Neurochem Int 23:115–122
Jarbe TU, Henriksson BG (1973) Effects of delta8-THC, and delta9-THC on the acquisition of a discriminative positional habit in rats. The transitions between normal and tetrahydrocannabinol-induced states on reversal learning. Psychopharmacologia 31:321–332
Joel D, Weiner I (2000) The connections of the dopaminergic system with the striatum in rats and primates: an analysis with respect to the functional and compartmental organization of the striatum. Neuroscience 96:451–474
Julian MD, Martin AB, Cuellar B, Rodriguez De Fonseca F, Navarro M, Moratalla R, Garcia-Segura LM (2003) Neuroanatomical relationship between type 1 cannabinoid receptors and dopaminergic systems in the rat basal ganglia. Neuroscience 119:309–318
Jung KM, Mangieri R, Stapleton C, Kim J, Fegley D, Wallace M, Mackie K, Piomelli D (2005) Stimulation of endocannabinoid formation in brain slice cultures through activation of group I metabotropic glutamate receptors. Mol Pharmacol 68:1196–1202
Kano M, Ohno-Shosaku T, Hashimotodani Y, Uchigashima M, Watanabe M (2009) Endocannabinoid-mediated control of synaptic transmission. Physiol Rev 89:309–380
Kathmann M, Bauer U, Schlicker E, Gothert 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
Katona I (2009) Endocannabinoid receptors: CNS localization of the CB(1) cannabinoid receptor. Curr Top Behav Neurosci 1:65–86
Kauer JA, Gibson HE (2009) Hot flash: TRPV channels in the brain. Trends Neurosci 32:215–224
Kawaguchi Y (1992) Large aspiny cells in the matrix of the rat neostriatum in vitro: physiological identification, relation to the compartments and excitatory postsynaptic currents. J Neurophysiol 67:1669–1682
Kawaguchi Y (1993) Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J Neurosci 13:4908–4923
Kheirbek MA, Britt JP, Beeler JA, Ishikawa Y, McGehee DS, Zhuang X (2009) Adenylyl cyclase type 5 contributes to corticostriatal plasticity and striatum-dependent learning. J Neurosci 29:12115–12124
Kim DS, Palmiter RD (2008) Interaction of dopamine and adenosine receptor function in behavior: studies with dopamine-deficient mice. Front Biosci 13:2311–2318
Kincaid AE, Wilson CJ (1996) Corticostriatal innervation of the patch and matrix in the rat neostriatum. J Comp Neurol 374:578–592
Kita H (1993) GABAergic circuits of the striatum. Prog Brain Res 99:51–72
Kobayashi K, Manabe T, Takahashi T (1999) Calcium-dependent mechanisms involved in presynaptic long-term depression at the hippocampal mossy fibre-CA3 synapse. Eur J Neurosci 11:1633–1638
Kofalvi A, Rodrigues RJ, Ledent C, Mackie K, Vizi ES, Cunha RA, Sperlagh B (2005) Involvement of cannabinoid receptors in the regulation of neurotransmitter release in the rodent striatum: a combined immunochemical and pharmacological analysis. J Neurosci 25:2874–2884
Koles L, Garcao P, Zadori ZS, Ferreira SG, Pinheiro BS, da Silva-Santos CS, Ledent C, Kofalvi A (2013) Presynaptic TRPV1 vanilloid receptor function is age- but not CB1 cannabinoid receptor-dependent in the rodent forebrain. Brain Res Bull 97:126–135
Koos T, Tepper JM (1999) Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat Neurosci 2:467–472
Kramer PF, Christensen CH, Hazelwood LA, Dobi A, Bock R, Sibley DR, Mateo Y, Alvarez VA (2011) Dopamine D2 receptor overexpression alters behavior and physiology in Drd2-EGFP mice. J Neurosci 31:126–132
Kreitzer AC, Malenka RC (2005) Dopamine modulation of state-dependent endocannabinoid release and long-term depression in the striatum. J Neurosci 25:10537–10545
Kreitzer AC, Malenka RC (2007) Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson’s disease models. Nature 445:643–647
Kreitzer AC, Malenka RC (2008) Striatal plasticity and basal ganglia circuit function. Neuron 60:543–554
Kreitzer AC, Regehr WG (2001) Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29:717–727
Kubota Y, Mikawa S, Kawaguchi Y (1993) Neostriatal GABAergic interneurones contain NOS, calretinin or parvalbumin. Neuroreport 5:205–208
Kushmerick C, Price GD, Taschenberger H, Puente N, Renden R, Wadiche JI, Duvoisin RM, Grandes P, von Gersdorff H (2004) Retroinhibition of presynaptic Ca2+ currents by endocannabinoids released via postsynaptic mGluR activation at a calyx synapse. J Neurosci 24:5955–5965
Langer LF, Graybiel AM (1989) Distinct nigrostriatal projection systems innervate striosomes and matrix in the primate striatum. Brain Res 498:344–350
Lerner TN, Kreitzer AC (2012) RGS4 is required for dopaminergic control of striatal LTD and susceptibility to parkinsonian motor deficits. Neuron 73:347–359
Lerner TN, Horne EA, Stella N, Kreitzer AC (2010) Endocannabinoid signaling mediates psychomotor activation by adenosine A2A antagonists. J Neurosci 30:2160–2164
Li ST, Kato K, Tomizawa K, Matsushita M, Moriwaki A, Matsui H, Mikoshiba K (2002) Calcineurin plays different roles in group II metabotropic glutamate receptor- and NMDA receptor-dependent long-term depression. J Neurosci 22:5034–5041
Ligresti A, Cascio MG, Di Marzo V (2005) Endocannabinoid metabolic pathways and enzymes. Curr Drug Targets CNS Neurol Disord 4:615–623
Liu J, Wang L, Harvey-White J, Osei-Hyiaman D, Razdan R, Gong Q, Chan AC, Zhou Z, Huang BX, Kim HY, Kunos G (2006) A biosynthetic pathway for anandamide. Proc Natl Acad Sci U S A 103:13345–13350
Lodge D, Tidball P, Mercier MS, Lucas SJ, Hanna L, Ceolin L, Kritikos M, Fitzjohn SM, Sherwood JL, Bannister N, Volianskis A, Jane DE, Bortolotto ZA, Collingridge GL (2013) Antagonists reversibly reverse chemical LTD induced by group I, group II and group III metabotropic glutamate receptors. Neuropharmacology 74:135–146
Lovinger DM, Tyler EC, Merritt A (1993) Short- and long-term synaptic depression in rat neostriatum. J Neurophysiol 70:1937–1949
Lovinger DM, Merritt A, Reyes D (1994) Involvement of N- and non-N-type calcium channels in synaptic transmission at corticostriatal synapses. Neuroscience 62:31–40
Lovinger DM, Davis MI, Costa RM (2010) Endocannabinoid signaling in the striatum. In: Steiner H, Tseng KY (eds) Handbook of behavioral neuroscience. Handbook of basal ganglia structure and function, vol 20. pp 167–186
Lupica CR, Riegel AC, Hoffman AF (2004) Marijuana and cannabinoid regulation of brain reward circuits. Br J Pharmacol 143:227–234
Maccarrone M, Attina M, Bari M, Cartoni A, Ledent C, Finazzi-Agro A (2001) Anandamide degradation and N-acylethanolamines level in wild-type and CB1 cannabinoid receptor knockout mice of different ages. J Neurochem 78:339–348
Maccarrone M, Gubellini P, Bari M, Picconi B, Battista N, Centonze D, Bernardi G, Finazzi-Agro A, Calabresi P (2003) Levodopa treatment reverses endocannabinoid system abnormalities in experimental parkinsonism. J Neurochem 85:1018–1025
Mackie K, Hille B (1992) Cannabinoids inhibit N-type calcium channels in neuroblastoma-glioma cells. Proc Natl Acad Sci U S A 89:3825–3829
Mackie K, Devane WA, Hille B (1993) Anandamide, an endogenous cannabinoid, inhibits calcium currents as a partial agonist in N18 neuroblastoma cells. Mol Pharmacol 44:498–503
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
Mailleux P, Vanderhaeghen JJ (1992a) Age-related loss of cannabinoid receptor binding sites and mRNA in the rat striatum. Neurosci Lett 147:179–181
Mailleux P, Vanderhaeghen JJ (1992b) Distribution of neuronal cannabinoid receptor in the adult rat brain: a comparative receptor binding radioautography and in situ hybridization histochemistry. Neuroscience 48:655–668
Malach R, Graybiel AM (1986) Mosaic architecture of the somatic sensory-recipient sector of the cat’s striatum. J Neurosci 6:3436–3458
Malinen H, Hyytiä P (2008) Ethanol self-administration is regulated by CB1 receptors in the nucleus accumbens and ventral tegmental area in alcohol-preferring AA rats. Alcohol Clin Exp Res 32(11):1976–1983
Malone DT, Kearn CS, Chongue L, Mackie K, Taylor DA (2008) Effect of social isolation on CB1 and D2 receptor and fatty acid amide hydrolase expression in rats. Neuroscience 152:265–272
Manzoni OJ, Bockaert J (2001) Cannabinoids inhibit GABAergic synaptic transmission in mice nucleus accumbens. Eur J Pharmacol 412:R3–R5
Marco EM, Echeverry-Alzate V, Lopez-Moreno JA, Gine E, Penasco S, Viveros MP (2014) Consequences of early life stress on the expression of endocannabinoid-related genes in the rat brain. Behav Pharmacol 25:547–556
Marshall K, Gowing L, Ali R, Le Foll B (2014) Pharmacotherapies for cannabis dependence. Cochrane Database Syst Rev 2:CD008940. doi:10.1002/14651858
Marsicano G, Lutz B (1999) Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain. Eur J Neurosci 11:4213–4225
Martin BR, Compton DR, Thomas BF, Prescott WR, Little PJ, Razdan RK, Johnson MR, Melvin LS, Mechoulam R, Ward SJ (1991) Behavioral, biochemical, and molecular modeling evaluations of cannabinoid analogs. Pharmacol Biochem Behav 40:471–478
Martin HGS, Bernabeu A, Lassalle O, Bouille C, Beurrier C, Pelissier-Alicot A-L, Manzoni OJ (2015) Endocannabinoids mediate muscarinic acetylcholine receptor-dependent long-term depression in the adult medial prefrontal cortex. Front Cell Neurosci 9:457. doi:10.3389/fncel.2015.00457
Martire A, Tebano MT, Chiodi V, Ferreira SG, Cunha RA, Kofalvi A, Popoli P (2011) Pre-synaptic adenosine A2A receptors control cannabinoid CB1 receptor-mediated inhibition of striatal glutamatergic neurotransmission. J Neurochem 116:273–280
Mathur BN, Tanahira C, Tamamaki N, Lovinger DM (2013) Voltage drives diverse endocannabinoid signals to mediate striatal microcircuit-specific plasticity. Nat Neurosci 16:1275–1283
Mato S, Chevaleyre V, Robbe D, Pazos A, Castillo PE, Manzoni OJ (2004) A single in-vivo exposure to delta 9THC blocks endocannabinoid-mediated synaptic plasticity. Nat Neurosci 7(6):585–586
Mato S, Robbe D, Puente N, Grandes P, Manzoni OJ (2005) Presynaptic homeostatic plasticity rescues long-term depression after chronic Delta 9-tetrahydrocannabinol exposure. J Neurosci 25:11619–11627
Mato S, Lafourcade M, Robbe D, Bakiri Y, Manzoni OJ (2008) Role of the cyclic-AMP/PKA cascade and of P/Q-type Ca++ channels in endocannabinoid-mediated long-term depression in the nucleus accumbens. Neuropharmacology 54:87–94
Matsuda LA, Lolait SJ, Brownstein MJ, Young AC, Bonner TI (1990) Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346:561–564
Matsuda LA, Bonner TI, Lolait SJ (1993) Localization of cannabinoid receptor mRNA in rat brain. J Comp Neurol 327:535–550
Matyas F, Watanabe M, Mackie K, Katona I, Freund TF (2007) Molecular architecture of the cannabinoid signaling system in the core of the nucleus accumbens. Ideggyogy Sz 60:187–191
McCutcheon JE, Loweth JA, Ford KA, Marinelli M, Wolf ME, Tseng KY (2011) Group I mGluR activation reverses cocaine-induced accumulation of calcium-permeable AMPA receptors in nucleus accumbens synapses via a protein kinase C-dependent mechanism. J Neurosci 31(41):14536–14541
Mechoulam R, Ben-Shabat S, Hanus L, Ligumsky M, Kaminski NE, Schatz AR, Gopher A, Almog S, Martin BR, Compton DR et al (1995) Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem Pharmacol 50:83–90
Micale V, Cristino L, Tamburella A, Petrosino S, Leggio GM, Drago F, Di Marzo V (2009) Anxiolytic effects in mice of a dual blocker of fatty acid amide hydrolase and transient receptor potential vanilloid type-1 channels. Neuropsychopharmacology 34:593–606
Monory K, Blaudzun H, Massa F, Kaiser N, Lemberger T, Schutz G, Wotjak CT, Lutz B, Marsicano G (2007) Genetic dissection of behavioural and autonomic effects of Delta(9)-tetrahydrocannabinol in mice. PLoS Biol 5:e269
Narushima M, Hashimoto K, Kano M (2006a) Endocannabinoid-mediated short-term suppression of excitatory synaptic transmission to medium spiny neurons in the striatum. Neurosci Res 54:159–164
Narushima M, Uchigashima M, Hashimoto K, Watanabe M, Kano M (2006b) Depolarization-induced suppression of inhibition mediated by endocannabinoids at synapses from fast-spiking interneurons to medium spiny neurons in the striatum. Eur J Neurosci 24:2246–2252
Narushima M, Uchigashima M, Fukaya M, Matsui M, Manabe T, Hashimoto K, Watanabe M, Kano M (2007) Tonic enhancement of endocannabinoid-mediated retrograde suppression of inhibition by cholinergic interneuron activity in the striatum. J Neurosci 27:496–506
Naydenov AV, Sepers MD, Swinney K, Raymond LA, Palmiter RD, Stella N (2014) Genetic rescue of CB1 receptors on medium spiny neurons prevents loss of excitatory striatal synapses but not motor impairment in HD mice. Neurobiol Dis 71:140–150
Nazzaro C, Greco B, Cerovic M, Baxter P, Rubino T, Trusel M, Parolaro D, Tkatch T, Benfenati F, Pedarzani P, Tonini R (2012) SK channel modulation rescues striatal plasticity and control over habit in cannabinoid tolerance. Nat Neurosci 15:284–293
Nyilas R, Dudok B, Urban GM, Mackie K, Watanabe M, Cravatt BF, Freund TF, Katona I (2008) Enzymatic machinery for endocannabinoid biosynthesis associated with calcium stores in glutamatergic axon terminals. J Neurosci 28:1058–1063
Nyiri G, Cserep C, Szabadits E, Mackie K, Freund TF (2005) CB1 cannabinoid receptors are enriched in the perisynaptic annulus and on preterminal segments of hippocampal GABAergic axons. Neuroscience 136:811–822
Okamoto Y, Morishita J, Tsuboi K, Tonai T, Ueda N (2004) Molecular characterization of a phospholipase D generating anandamide and its congeners. J Biol Chem 279:5298–5305
Okamoto Y, Wang J, Morishita J, Ueda N (2007) Biosynthetic pathways of the endocannabinoid anandamide. Chem Biodivers 4:1842–1857
Olson PA, Tkatch T, Hernandez-Lopez S, Ulrich S, Ilijic E, Mugnaini E, Zhang H, Bezprozvanny I, Surmeier DJ (2005) G-protein-coupled receptor modulation of striatal CaV1.3 L-type Ca2+ channels is dependent on a Shank-binding domain. J Neurosci 25:1050–1062
Orio L, Edwards S, George O, Parsons LH, Koob GF (2009) A role for the endocannabinoid system in the increased motivation for cocaine in extended-access conditions. J Neurosci 29(15):4846–4857
Ortinski PI, Vassoler FM, Carlson GC, Pierce RC (2012) Temporally dependent changes in cocaine-induced synaptic plasticity in the nucleus accumbens shell are reversed by D1-like dopamine receptor stimulation. Neuropsychopharmacology 37(7):1671–1682
Oude Ophuis RJ, Boender AJ, van Rozen AJ, Adan RA (2014) Cannabinoid, melanocortin and opioid receptor expression on DRD1 and DRD2 subpopulations in rat striatum. Front Neuroanat 8:14
Packard MG, McGaugh JL (1996) Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol Learn Mem 65:65–72
Palazuelos J, Aguado T, Pazos MR, Julien B, Carrasco C, Resel E, Sagredo O, Benito C, Romero J, Azcoitia I, Fernandez-Ruiz J, Guzman M, Galve-Roperh I (2009) Microglial CB2 cannabinoid receptors are neuroprotective in Huntington’s disease excitotoxicity. Brain 132:3152–3164
Parsons LH, Hurd YL (2015) Endocannabinoid signalling in reward and addiction. Nat Rev Neurosci 16:579–594
Partridge JG, Janssen MJ, Chou DY, Abe K, Zukowska Z, Vicini S (2009) Excitatory and inhibitory synapses in neuropeptide Y-expressing striatal interneurons. J Neurophysiol 102:3038–3045
Perez-Burgos A, Perez-Rosello T, Salgado H, Flores-Barrera E, Prieto GA, Figueroa A, Galarraga E, Bargas J (2008) Muscarinic M(1) modulation of N and L types of calcium channels is mediated by protein kinase C in neostriatal neurons. Neuroscience 155:1079–1097
Perra S, Pillolla G, Melis M, Muntoni AL, Gessa GL, Pistis M (2005) Involvement of the endogenous cannabinoid system in the effects of alcohol in the mesolimbic reward circuit: electrophysiological evidence in vivo. Psychopharmacology 183(3):368–377
Pertwee RG (2015) Endocannabinoids and their pharmacological actions. Handb Exp Pharmacol 231:1–37
Pertwee RG, Wickens AP (1991) Enhancement by chlordiazepoxide of catalepsy induced in rats by intravenous or intrapallidal injections of enantiomeric cannabinoids. Neuropharmacology 30:237–244
Petryszyn S, Beaulieu JM, Parent A, Parent M (2014) Distribution and morphological characteristics of striatal interneurons expressing calretinin in mice: a comparison with human and nonhuman primates. J Chem Neuroanat 59-60:51–61
Picconi B, Bagetta V, Ghiglieri V, Paille V, Di Filippo M, Pendolino V, Tozzi A, Giampa C, Fusco FR, Sgobio C, Calabresi P (2011) Inhibition of phosphodiesterases rescues striatal long-term depression and reduces levodopa-induced dyskinesia. Brain 134:375–387
Pickel VM, Chan J, Kash TL, Rodriguez JJ, MacKie K (2004) Compartment-specific localization of cannabinoid 1 (CB1) and mu-opioid receptors in rat nucleus accumbens. Neuroscience 127:101–112
Pickel VM, Chan J, Kearn CS, Mackie K (2006) Targeting dopamine D2 and cannabinoid-1 (CB1) receptors in rat nucleus accumbens. J Comp Neurol 495:299–313
Pickel VM, Shobin ET, Lane DA, Mackie K (2012) Cannabinoid-1 receptors in the mouse ventral pallidum are targeted to axonal profiles expressing functionally opposed opioid peptides and contacting N-acylphosphatidylethanolamine-hydrolyzing phospholipase D terminals. Neuroscience 227:10–21
Piomelli D, Giuffrida A, Calignano A, Rodriguez de Fonseca F (2000) The endocannabinoid system as a target for therapeutic drugs. Trends Pharmacol Sci 21:218–224
Quiroz C, Lujan R, Uchigashima M, Simoes AP, Lerner TN, Borycz J, Kachroo A, Canas PM, Orru M, Schwarzschild MA, Rosin DL, Kreitzer AC, Cunha RA, Watanabe M, Ferre S (2009) Key modulatory role of presynaptic adenosine A2A receptors in cortical neurotransmission to the striatal direct pathway. ScientificWorldJournal 9:1321–1344
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
Robbe D, Alonso G, Chaumont S, Bockaert J, Manzoni OJ (2002a) Role of p/q-Ca2+ channels in metabotropic glutamate receptor 2/3-dependent presynaptic long-term depression at nucleus accumbens synapses. J Neurosci 22:4346–4356
Robbe D, Kopf M, Remaury A, Bockaert J, Manzoni OJ (2002b) Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc Natl Acad Sci U S A 99:8384–8388
Roberts JC, Davis JB, Benham CD (2004) [3H]Resiniferatoxin autoradiography in the CNS of wild-type and TRPV1 null mice defines TRPV1 (VR-1) protein distribution. Brain Res 995:176–183
Rodriguez JJ, Mackie K, Pickel VM (2001) Ultrastructural localization of the CB1 cannabinoid receptor in mu-opioid receptor patches of the rat Caudate putamen nucleus. J Neurosci 21:823–833
Rodriguez-Moreno A, Banerjee A, Paulsen O (2010) Presynaptic NMDA receptors and spike timing-dependent depression at cortical synapses. Front Synaptic Neurosci 2:18
Romero J, Garcia-Palomero E, Castro JG, Garcia-Gil L, Ramos JA, Fernandez-Ruiz JJ (1997) Effects of chronic exposure to delta9-tetrahydrocannabinol on cannabinoid receptor binding and mRNA levels in several rat brain regions. Brain Res Mol Brain Res 46:100–108
Ronesi J, Lovinger DM (2005) Induction of striatal long-term synaptic depression by moderate frequency activation of cortical afferents in rat. J Physiol 562:245–256
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 24:1673–1679
Sagredo O, Gonzalez S, Aroyo I, Pazos MR, Benito C, Lastres-Becker I, Romero JP, Tolon RM, Mechoulam R, Brouillet E, Romero J, Fernandez-Ruiz J (2009) Cannabinoid CB2 receptor agonists protect the striatum against malonate toxicity: relevance for Huntington’s disease. Glia 57:1154–1167
Seif T, Makriyannis A, Kunos G, Bonci A, Hopf FW (2011) The endocannabinoid 2-arachidonoylglycerol mediates D1 and D2 receptor cooperative enhancement of rat nucleus accumbens core neuron firing. Neuroscience 193:21–33
Sergeeva OA, Doreulee N, Chepkova AN, Kazmierczak T, Haas HL (2007) Long-term depression of cortico-striatal synaptic transmission by DHPG depends on endocannabinoid release and nitric oxide synthesis. Eur J Neurosci 26:1889–1894
Shen M, Thayer SA (1998) The cannabinoid agonist Win55,212-2 inhibits calcium channels by receptor-mediated and direct pathways in cultured rat hippocampal neurons. Brain Res 783:77–84
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
Shen W, Flajolet M, Greengard P, Surmeier DJ (2008) Dichotomous dopaminergic control of striatal synaptic plasticity. Science 321:848–851
Shonesy BC, Wang X, Rose KL, Ramikie TS, Cavener VS, Rentz T, Baucum AJ 2nd, Jalan-Sakrikar N, Mackie K, Winder DG, Patel S, Colbran RJ (2013) CaMKII regulates diacylglycerol lipase-alpha and striatal endocannabinoid signaling. Nat Neurosci 16:456–463
Shonesy BC, Winder DG, Patel S, Colbran RJ (2015) The initiation of synaptic 2-AG mobilization requires both an increased supply of diacylglycerol precursor and increased postsynaptic calcium. Neuropharmacology 91:57–62
Sidlo Z, Reggio PH, Rice ME (2008) Inhibition of striatal dopamine release by CB1 receptor activation requires nonsynaptic communication involving GABA, H2O2, and KATP channels. Neurochem Int 52:80–88
Simon GM, Cravatt BF (2006) Endocannabinoid biosynthesis proceeding through glycerophospho-N-acyl ethanolamine and a role for alpha/beta-hydrolase 4 in this pathway. J Biol Chem 281:26465–26472
Simon GM, Cravatt BF (2008) Anandamide biosynthesis catalyzed by the phosphodiesterase GDE1 and detection of glycerophospho-N-acyl ethanolamine precursors in mouse brain. J Biol Chem 283:9341–9349
Simon GM, Cravatt BF (2010) Characterization of mice lacking candidate N-acyl ethanolamine biosynthetic enzymes provides evidence for multiple pathways that contribute to endocannabinoid production in vivo. Mol BioSyst 6:1411–1418
Singla S, Kreitzer AC, Malenka RC (2007) Mechanisms for synapse specificity during striatal long-term depression. J Neurosci 27:5260–5264
Smart D, Jerman JC (2000) Anandamide: an endogenous activator of the vanilloid receptor. Trends Pharmacol Sci 21:134
Song WJ, Tkatch T, Surmeier DJ (2000) Adenosine receptor expression and modulation of Ca(2+) channels in rat striatal cholinergic interneurons. J Neurophysiol 83:322–332
Soria-Gomez E, Matias I, Rueda-Orozco PE, Cisneros M, Petrosino S, Navarro L, Di Marzo V, Prospero-Garcia O (2007) Pharmacological enhancement of the endocannabinoid system in the nucleus accumbens shell stimulates food intake and increases c-Fos expression in the hypothalamus. Br J Pharmacol 151:1109–1116
Stanton PK, Gage AT (1996) Distinct synaptic loci of Ca2+/calmodulin-dependent protein kinase II necessary for long-term potentiation and depression. J Neurophysiol 76:2097–2101
Starowicz K, Cristino L, Di Marzo V (2008) TRPV1 receptors in the central nervous system: potential for previously unforeseen therapeutic applications. Curr Pharm Des 14:42–54
Stella N, Schweitzer P, Piomelli D (1997) A second endogenous cannabinoid that modulates long-term potentiation. Nature 388:773–778
Stromberg I, Popoli P, Muller CE, Ferre S, Fuxe K (2000) Electrophysiological and behavioural evidence for an antagonistic modulatory role of adenosine A2A receptors in dopamine D2 receptor regulation in the rat dopamine-denervated striatum. Eur J Neurosci 12:4033–4037
Sugiura T, Kondo S, Sukagawa A, Nakane S, Shinoda A, Itoh K, Yamashita A, Waku K (1995) 2-Arachidonoylglycerol: a possible endogenous cannabinoid receptor ligand in brain. Biochem Biophys Res Commun 215:89–97
Sung KW, Choi S, Lovinger DM (2001) Activation of group I mGluRs is necessary for induction of long-term depression at striatal synapses. J Neurophysiol 86:2405–2412
Svenningsson P, Le Moine C, Kull B, Sunahara R, Bloch B, Fredholm BB (1997) Cellular expression of adenosine A2A receptor messenger RNA in the rat central nervous system with special reference to dopamine innervated areas. Neuroscience 80:1171–1185
Szabo B, Dorner L, Pfreundtner C, Norenberg W, Starke K (1998) Inhibition of GABAergic inhibitory postsynaptic currents by cannabinoids in rat corpus striatum. Neuroscience 85:395–403
Szabo B, Muller 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
Tanda G, Munzar P, Goldberg SR (2000) Self-administration behavior is maintained by the psychoactive ingredient of marijuana in squirrel monkeys. Nat Neurosci 3:1073–1107
Tang K, Low MJ, Grandy DK, Lovinger DM (2001) Dopamine-dependent synaptic plasticity in striatum during in vivo development. Proc Natl Acad Sci U S A 98:1255–1260
Tanimura A, Yamazaki M, Hashimotodani Y, Uchigashima M, Kawata S, Abe M, Kita Y, Hashimoto K, Shimizu T, Watanabe M, Sakimura K, Kano M (2010) The endocannabinoid 2-arachidonoylglycerol produced by diacylglycerol lipase alpha mediates retrograde suppression of synaptic transmission. Neuron 65:320–327
Tepper JM, Bolam JP (2004) Functional diversity and specificity of neostriatal interneurons. Curr Opin Neurobiol 14:685–692
Tepper JM, Abercrombie ED, Bolam JP (2007) Basal ganglia macrocircuits. Prog Brain Res 160:3–7
Tepper JM, Tecuapetla F, Koos T, Ibanez-Sandoval O (2010) Heterogeneity and diversity of striatal GABAergic interneurons. Front Neuroanat 4:150
Thiemann G, van der Stelt M, Petrosino S, Molleman A, Di Marzo V, Hasenohrl RU (2008) The role of the CB1 cannabinoid receptor and its endogenous ligands, anandamide and 2-arachidonoylglycerol, in amphetamine-induced behavioural sensitization. Behav Brain Res 187:289–296
Tozzi A, Tscherter A, Belcastro V, Tantucci M, Costa C, Picconi B, Centonze D, Calabresi P, Borsini F (2007) Interaction of A2A adenosine and D2 dopamine receptors modulates corticostriatal glutamatergic transmission. Neuropharmacology 53:783–789
Tozzi A, de Iure A, Di Filippo M, Tantucci M, Costa C, Borsini F, Ghiglieri V, Giampa C, Fusco FR, Picconi B, Calabresi P (2011) The distinct role of medium spiny neurons and cholinergic interneurons in the D(2)/A(2)A receptor interaction in the striatum: implications for Parkinson’s disease. J Neurosci 31:1850–1862
Tozzi A, de Iure A, Marsili V, Romano R, Tantucci M, Di Filippo M, Costa C, Napolitano F, Mercuri NB, Borsini F, Giampa C, Fusco FR, Picconi B, Usiello A, Calabresi P (2012) A2A adenosine receptor antagonism enhances synaptic and motor effects of cocaine via CB1 cannabinoid receptor activation. PLoS One 7:e38312
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
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
Uchigashima M, Narushima M, Fukaya M, Katona I, Kano M, Watanabe M (2007) Subcellular arrangement of molecules for 2-arachidonoyl-glycerol-mediated retrograde signaling and its physiological contribution to synaptic modulation in the striatum. J Neurosci 27:3663–3676
Ueda N, Kurahashi Y, Yamamoto S, Tokunaga T (1995) Partial purification and characterization of the porcine brain enzyme hydrolyzing and synthesizing anandamide. J Biol Chem 270:23823–23827
Valjent E, Maldonado R (2000) A behavioural model to reveal place preference to delta 9-tetrahydrocannabinol in mice. Psychopharmacology (Berl) 147:436–438
Van Waes V, Beverley JA, Siman H, Tseng KY, Steiner H (2012) CB1 cannabinoid receptor expression in the striatum: association with corticostriatal circuits and developmental regulation. Front Pharmacol 3:21
Volkow ND, Wang GJ, Telang F, Fowler JS, Alexoff D, Logan J, Jayne M, Wong C, Tomasi D (2014) Decreased dopamine brain reactivity in marijuana abusers is associated with negative emotionality and addiction severity. Proc Natl Acad Sci U S A 111(30):E3149–E3156
Walsh JP (1993) Depression of excitatory synaptic input in rat striatal neurons. Brain Res 608:123–128
Wang H, Pickel VM (2002) Dopamine D2 receptors are present in prefrontal cortical afferents and their targets in patches of the rat caudate-putamen nucleus. J Comp Neurol 442:392–404
Wang Z, Kai L, Day M, Ronesi J, Yin HH, Ding J, Tkatch T, Lovinger DM, Surmeier DJ (2006) Dopaminergic control of corticostriatal long-term synaptic depression in medium spiny neurons is mediated by cholinergic interneurons. Neuron 50:443–452
Wang W, Dever D, Lowe J, Storey GP, Bhansali A, Eck EK, Nitulescu I, Weimer J, Bamford NS (2012) Regulation of prefrontal excitatory neurotransmission by dopamine in the nucleus accumbens core. J Physiol 590:3743–3769
Wilson RI, Nicoll RA (2001) Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410:588–592
Wilson RI, Nicoll RA (2002) Endocannabinoid signaling in the brain. Science 296:678–682
Winters BD, Kruger JM, Huang X, Gallaher ZR, Ishikawa M, Czaja K, Krueger JM, Huang YH, Schluter OM, Dong Y (2012) Cannabinoid receptor 1-expressing neurons in the nucleus accumbens. Proc Natl Acad Sci U S A 109:E2717–E2725
Wong MY, Borgkvist A, Choi SJ, Mosharov EV, Bamford NS, Sulzer D (2015) Dopamine-dependent corticostriatal synaptic filtering regulates sensorimotor behavior. Neuroscience 290:594–607
Wu YW, Kim JI, Tawfik VL, Lalchandani RR, Scherrer G, Ding JB (2015) Input- and cell-type-specific endocannabinoid-dependent LTD in the striatum. Cell Rep 10:75–87
Xi ZX, Gilbert JG, Peng XQ, Pak AC, Li X, Gardner EL (2006) Cannabinoid CB1 receptor antagonist AM251 inhibits cocaine-primed relapse in rats: role of glutamate in the nucleus accumbens. J Neurosci 26(33):8531–8536
Xi ZX, Peng XQ, Li X, Song R, Zhang HY, Liu QR, Yang HJ, Bi GH, Li J, Gardner EL (2011) Brain cannabinoid CB2 receptors modulate cocaine’s actions in mice. Nat Neurosci 14(9):1160–1166
Xia JX, Li J, Zhou R, Zhang XH, Ge YB, Ru Yuan X (2006) Alterations of rat corticostriatal synaptic plasticity after chronic ethanol exposure and withdrawal. Alcohol Clin Exp Res 30:819–824
Yin HH, Knowlton BJ (2006) The role of the basal ganglia in habit formation. Nat Rev Neurosci 7(6):464–476
Yin HH, Lovinger DM (2006) Frequency-specific and D2 receptor-mediated inhibition of glutamate release by retrograde endocannabinoid signaling. Proc Natl Acad Sci U S A 103:8251–8256
Yin HH, Davis MI, Ronesi JA, Lovinger DM (2006) The role of protein synthesis in striatal long-term depression. J Neurosci 26:11811–11820
Yin HH, Adermark L, Lovinger DM (2008) Neurotensin reduces glutamatergic transmission in the dorsolateral striatum via retrograde endocannabinoid signaling. Neuropharmacology 54:79–86
Zangen A, Solinas M, Ikemoto S, Goldberg SR, Wise RA (2006) Two brain sites for cannabinoid reward. J Neurosci 26(18):4901–4907
Zhang X, Feng ZJ, Chergui K (2015) Induction of cannabinoid- and N-methyl-D-aspartate receptor-mediated long-term depression in the nucleus accumbens and dorsolateral striatum is region and age dependent. Int J Neuropsychopharmacol 18(4). doi:10.1093/ijnp/pyu052
Zhou FM, Wilson CJ, Dani JA (2002) Cholinergic interneuron characteristics and nicotinic properties in the striatum. J Neurobiol 53:590–605
Zygmunt PM, Petersson J, Andersson DA, Chuang H, Sorgard M, Di Marzo V, Julius D, Hogestatt ED (1999) Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400:452–457
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing AG
About this chapter
Cite this chapter
Atwood, B.K., Lovinger, D.M. (2017). Endocannabinoid-Dependent Synaptic Plasticity in the Striatum. In: Melis, M. (eds) Endocannabinoids and Lipid Mediators in Brain Functions. Springer, Cham. https://doi.org/10.1007/978-3-319-57371-7_5
Download citation
DOI: https://doi.org/10.1007/978-3-319-57371-7_5
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-57369-4
Online ISBN: 978-3-319-57371-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)