Skip to main content
SpringerLink
Log in

Cannabinoid Modulation of Dopaminergic Circuits in Neurodegenerative and Neuropsychiatric Disorders

  • Chapter
  • First Online:
Endocannabinoid Regulation of Monoamines in Psychiatric and Neurological Disorders

Abstract

The endocannabinoid system timely orchestrates a variety of cerebral physiological processes by modulating brain neurotransmitters, and in particular the dopamine system. Both endocannabinoid and dopamine receptors are highly abundant and often coexpressed in the basal ganglia and mesolimbic pathways, where they regulate motor functions and motivational aspects of behavior. Understanding the interrelationship between these two systems is crucial to gain new insight on the pathophysiology of brain disorders characterized by a dysregulation of dopamine, such as Parkinson’s disease and schizophrenia. This review aims at: (1) presenting the complex functional interactions between these two neurotransmitter systems at the anatomical, pharmacological, cellular and electrophysiological levels, and (2) addressing the contribution of disturbances of cannabinoid–dopamine interactions to neurodegenerative and psychiatric disorders.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

2-AG:

2-arachidonoylglycerol

CNS:

central nervous system

GABA:

γ-aminobutyric acid

NAPE-PLD:

N-acyl phosphatidylethanolamine phospholipase D

FAAH:

fatty acid amide hydrolase

MAGL:

monoacylglycerol lipase

DAGL:

diacylglycerol lipase

DSE:

depolarization-induced suppression of excitation

DSI:

depolarization-induced suppression of inhibition

STD:

short-term depression

PFC:

prefrontal cortex

LTP:

long-term potentiation

LTD:

long-term depression

THC:

tetrahydrocannabinol

CB1:

cannabinoid receptor 1

D1R:

dopamine receptor 1

PD:

Parkinson’s disease

D2R:

dopamine receptor 1

KO:

knock-out

LID:

L-dopa induced dyskinesia

6-OHDA:

6-hydroxydopamine

MPTP:

(1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine)

VTA:

ventral tegmental area

ECS:

endocannabinoid system

References

  • Ahn K, McKinney MK, Cravatt BF (2008) Enzymatic pathways that regulate endocannabinoid signaling in the nervous system. Chem Rev 108:1687–1707

    Article  PubMed  CAS  Google Scholar 

  • Ameri A (1999) The effects of cannabinoids on the brain. Prog Neurobiol 58:315–348

    Article  PubMed  CAS  Google Scholar 

  • Anderson JJ, Kask AM, Chase TN (1996) Effects of cannabinoid receptor stimulation and blockade on catalepsy produced by dopamine receptor antagonists. Eur J Pharmacol 295:163–168

    Article  PubMed  CAS  Google Scholar 

  • Andre VM, Cepeda C, Cummings DM, Jocoy EL, Fisher YE, William Yang X, Levine MS (2010) Dopamine modulation of excitatory currents in the striatum is dictated by the expression of D1 or D2 receptors and modified by endocannabinoids. Eur J Neurosci 31:14–28

    Article  PubMed  Google Scholar 

  • Balazsa T, Biro J, Gullai N, Ledent C, Sperlagh B (2008) CB1-cannabinoid receptors are involved in the modulation of non-synaptic [3H]serotonin release from the rat hippocampus. Neurochem Int 52:95–102

    Article  PubMed  CAS  Google Scholar 

  • Basavarajappa BS (2007) Critical enzymes involved in endocannabinoid metabolism. Protein Pept Lett 14:237–246

    Article  PubMed  CAS  Google Scholar 

  • Beaulieu JM, Gainetdinov RR (2011) The physiology, signaling, and pharmacology of dopamine receptors. Pharmacol Rev 63:182–217

    Article  PubMed  CAS  Google Scholar 

  • Beltramo M, Fonseca FR de, Navarro M, Calignano A, Gorriti MA, Grammatikopoulos G, Sadile AG, Giuffrida A, Piomelli D (2000) Reversal of dopamine D(2) receptor responses by an anandamide transport inhibitor. J Neurosci 20:3401–3407

    PubMed  CAS  Google Scholar 

  • Bouaboula M, Poinot-Chazel C, Bourrie B, Canat X, Calandra B, Rinaldi-Carmona M, Le Fur G, Casellas P (1995) Activation of mitogen-activated protein kinase by stimulation of the central cannabinoid receptor CB1. Biochem J 312:637–641

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Cabral GA, Marciano-Cabral F (2005) Cannabinoid receptors in microglia of the central nervous system: immune functional relevance. J Leukoc Biol 78:1192–1197

    Article  PubMed  CAS  Google Scholar 

  • Cachope R (2012) Functional diversity on synaptic plasticity mediated by endocannabinoids. Philos Trans R Soc Lond B Biol Sci 367:3242–3253

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Cao X, Liang L, Hadcock JR, Iredale PA, Griffith DA, Menniti FS, Factor S, Greenamyre JT, Papa SM (2007) Blockade of cannabinoid type 1 receptors augments the antiparkinsonian action of levodopa without affecting dyskinesias in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated rhesus monkeys. J Pharmacol Exp Ther 323:318–326

    Article  PubMed  CAS  Google Scholar 

  • Carriba P, Ortiz O, Patkar K, Justinova Z, Stroik J, Themann A, Muller C, Woods AS, Hope BT, Ciruela F, Casado V, Canela EI, Lluis C, Goldberg SR, Moratalla R, Franco R, Ferre S (2007) Striatal adenosine A2A and cannabinoid CB1 receptors form functional heteromeric complexes that mediate the motor effects of cannabinoids. Neuropsychopharmacology 32:2249–2259

    Article  PubMed  CAS  Google Scholar 

  • Carroll CB, Bain PG, Teare L, Liu X, Joint C, Wroath BA, Parkin SG, Fox P, Wright D, Hobart J, Zajicek JP (2004) Cannabis for dyskinesia in Parkinson disease. Neurology 63:1245–1250

    Article  PubMed  CAS  Google Scholar 

  • Castellano C, Cabib S, Palmisano A, Di Marzo V, Puglisi-Allegra S (1997) The effects of anandamide on memory consolidation in mice involve both D1 and D2 dopamine receptors. Behav Pharmacol 8:707–712

    Article  PubMed  CAS  Google Scholar 

  • Cave JW, Baker H (2009) Dopamine systems in the forebrain. Adv Exp Med Biol 651:15–35

    Article  PubMed  CAS  Google Scholar 

  • Centonze D, Battista N, Rossi S, Mercuri NB, Finazzi-Agro A, Bernardi G, Calabresi P, Maccarrone M (2004) A critical interaction between dopamine D2 receptors and endocannabinoids mediates the effects of cocaine on striatal gabaergic Transmission. Neuropsychopharmacology 29:1488–1497

    Article  PubMed  CAS  Google Scholar 

  • Cheer JF, Kendall DA, Mason R, Marsden CA (2003) Differential cannabinoid-induced electrophysiological effects in rat ventral tegmentum. Neuropharmacology 44:633–641

    Article  PubMed  CAS  Google Scholar 

  • Chen J, Paredes W, Lowinson JH, Gardner EL (1990a) Delta 9-tetrahydrocannabinol enhances presynaptic dopamine efflux in medial prefrontal cortex. Eur J Pharmacol 190:259–262

    Article  CAS  Google Scholar 

  • Chen JP, Paredes W, Li J, Smith D, Lowinson J, Gardner EL (1990b) Delta 9-tetrahydrocannabinol produces naloxone-blockable enhancement of presynaptic basal dopamine efflux in nucleus accumbens of conscious, freely-moving rats as measured by intracerebral microdialysis. Psychopharmacology (Berl) 102:156–162

    Article  CAS  Google Scholar 

  • Chevaleyre V, Takahashi KA, Castillo PE (2006) Endocannabinoid-mediated synaptic plasticity in the CNS. Annu Rev Neurosci 29:37–76

    Article  PubMed  CAS  Google Scholar 

  • Chiu CQ, Puente N, Grandes P, Castillo PE (2010) Dopaminergic modulation of endocannabinoid-mediated plasticity at GABAergic synapses in the prefrontal cortex. J Neurosci 30:7236–7248

    Article  PubMed  CAS  Google Scholar 

  • Compton DR, Aceto MD, Lowe J, Martin BR (1996) In vivo characterization of a specific cannabinoid receptor antagonist (SR141716A): inhibition of D9-tetrahydrocannabinol-induced responses and apparent agonist activity. J Pharmacol Exp Ther 277:586–594

    PubMed  CAS  Google Scholar 

  • Compton DR, Martin BR (1997) The effect of the enzyme inhibitor phenylmethylsulfonyl fluoride on the pharmacological effect of anandamide in the mouse model of cannabimimetic activity. J Pharmacol Exp Ther 283:1138–1143

    PubMed  CAS  Google Scholar 

  • Console-Bram L, Marcu J, Abood ME (2012) Cannabinoid receptors: nomenclature and pharmacological principles. Prog Neuropsychopharmacol Biol Psychiatry 38:4–15

    Article  PubMed  CAS  Google Scholar 

  • Cools R (2011) Dopaminergic control of the striatum for high-level cognition. Curr Opin Neurobiol 21:402–407

    Article  PubMed  CAS  Google Scholar 

  • Cortright JJ, Lorrain DS, Beeler JA, Tang WJ, Vezina P (2011) Previous exposure to delta9-tetrahydrocannibinol enhances locomotor responding to but not self-administration of amphetamine. J Pharmacol Exp Ther 337:724–733

    Article  PubMed  CAS  Google Scholar 

  • Costain WF (2008) The effects of cannabis abuse on the symptoms of schizophrenia: patient perspectives. Int J Ment Health Nurs 17:227–235

    Article  PubMed  Google Scholar 

  • Costanzi M, Battaglia M, Rossi-Arnaud C, Cestari V, Castellano C (2004) Effects of anandamide and morphine combinations on memory consolidation in cd1 mice: involvement of dopaminergic mechanisms. Neurobiol Learn Mem 81:144–149

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Crean RD, Crane NA, Mason BJ (2011) An evidence based review of acute and long-term effects of cannabis use on executive cognitive functions. J Addict Med 5:1–8

    Article  PubMed  Google Scholar 

  • Curley AA, Lewis DA (2012) Cortical basket cell dysfunction in schizophrenia. J Physiol 590:715–724

    PubMed  CAS  Google Scholar 

  • D’Souza DC (2007) Cannabinoids and psychosis. Int Rev Neurobiol 78:289–326

    Article  PubMed  CAS  Google Scholar 

  • D’Souza DC, Perry E, MacDougall L, Ammerman Y, Cooper T, Wu YT, Braley G, Gueorguieva R, Krystal JH (2004) The psychotomimetic effects of intravenous delta-9-tetrahydrocannabinol in healthy individuals: implications for psychosis. Neuropsychopharmacology 29:1558–1572

    Article  PubMed  CAS  Google Scholar 

  • D’Souza DC, Sewell RA, Ranganathan M (2009) Cannabis and psychosis/schizophrenia: human studies. Eur Arch Psychiatry Clin Neurosci 259:413–431

    Article  PubMed  Google Scholar 

  • Dalton VS, Long LE, Weickert CS, Zavitsanou K (2011) Paranoid schizophrenia is characterized by increased CB1 receptor binding in the dorsolateral prefrontal cortex. Neuropsychopharmacology 36:1620–1630

    Article  PubMed  CAS  Google Scholar 

  • Lago E de, Miguel R de, Lastres-Becker I, Ramos JA, Fernandez-Ruiz J (2004) Involvement of vanilloid-like receptors in the effects of anandamide on motor behavior and nigrostriatal dopaminergic activity: in vivo and in vitro evidence. Brain Res 1007:152–159

    Article  PubMed  CAS  Google Scholar 

  • Dean B, Sundram S, Bradbury R, Scarr E, Copolov D (2001) Studies on [3H]CP-55940 binding in the human central nervous system: regional specific changes in density of cannabinoid-1 receptors associated with schizophrenia and cannabis use. Neuroscience 103:9–15

    Article  PubMed  CAS  Google Scholar 

  • Degroot A, Kofalvi A, Wade MR, Davis RJ, Rodrigues RJ, Rebola N, Cunha RA, Nomikos GG (2006) CB1 receptor antagonism increases hippocampal acetylcholine release: site and mechanism of action. Mol Pharmacol 70:1236–1245

    Article  PubMed  CAS  Google Scholar 

  • Demuth DG, Molleman A (2006) Cannabinoid signalling. Life Sci 78:549–563

    Article  PubMed  CAS  Google Scholar 

  • Derkinderen P, Valjent E, Toutant M, Corvol JC, Enslen H, Ledent C, Trzaskos J, Caboche J, Girault JA (2003) Regulation of extracellular signal-regulated kinase by cannabinoids in hippocampus. J Neurosci 23:2371–2382

    PubMed  CAS  Google Scholar 

  • Di Marzo V, Hill MP, Bisogno T, Crossman AR, Brotchie JM (2000) Enhanced levels of endogenous cannabinoids in the globus pallidus are associated with a reduction in movement in an animal model of Parkinson’s disease. FASEB J 14:1432–1438

    Article  PubMed  CAS  Google Scholar 

  • Dinh TP, Carpenter D, Leslie FM, Freund TF, Katona I, Sensi SL, Kathuria S, Piomelli D (2002) Brain monoglyceride lipase participating in endocannabinoid inactivation. Proc Natl Acad Sci U S A 99:10819–10824

    Article  PubMed  CAS  Google Scholar 

  • Dubreucq S, Matias I, Cardinal P, Haring M, Lutz B, Marsicano G, Chaouloff F (2012) Genetic dissection of the role of cannabinoid type-1 receptors in the emotional consequences of repeated social stress in mice. Neuropsychopharmacology 37:1885–1900

    Article  PubMed  CAS  Google Scholar 

  • Egerton A, Allison C, Brett RR, Pratt JA (2006) Cannabinoids and prefrontal cortical function: insights from preclinical studies. Neurosci Biobehav Rev 30:680–695

    Article  PubMed  CAS  Google Scholar 

  • Eggan SM, Hashimoto T, Lewis DA (2008) Reduced cortical cannabinoid 1 receptor messenger RNA and protein expression in schizophrenia. Arch Gen Psychiatry 65:772–784

    Article  PubMed  Google Scholar 

  • Eggan SM, Stoyak SR, Verrico CD, Lewis DA (2010) Cannabinoid CB1 receptor immunoreactivity in the prefrontal cortex: comparison of schizophrenia and major depressive disorder. Neuropsychopharmacology 35:2060–2071

    Article  PubMed  CAS  Google Scholar 

  • Ellis J, Pediani JD, Canals M, Milasta S, Milligan G (2006) Orexin-1 receptor-cannabinoid CB1 receptor heterodimerization results in both ligand-dependent and -independent coordinated alterations of receptor localization and function. J Biol Chem 281:38812–38824

    Article  PubMed  CAS  Google Scholar 

  • Esteban S, Garcia-Sevilla JA (2012) Effects induced by cannabinoids on monoaminergic systems in the brain and their implications for psychiatric disorders. Prog Neuropsychopharmacol Biol Psychiatry 38:78–87

    Article  PubMed  CAS  Google Scholar 

  • Fabbrini G, Brotchie JM, Grandas F, Nomoto M, Goetz CG (2007) Levodopa-induced dyskinesias. Mov Disord 22:1379–1389; quiz 1523

    Google Scholar 

  • Fadda P, Scherma M, Spano MS, Salis P, Melis V, Fattore L, Fratta W (2006) Cannabinoid self-administration increases dopamine release in the nucleus accumbens. Neuroreport 17:1629–1632

    Article  PubMed  CAS  Google Scholar 

  • Fattore L, Melis M, Fadda P, Pistis M, Fratta W (2010) The endocannabinoid system and nondrug rewarding behaviours. Exp Neurol 224:23–36

    Article  PubMed  CAS  Google Scholar 

  • Fernandez-Espejo E, Caraballo I, Rodriguez de Fonseca F, El Banoua F, Ferrer B, Flores JA, Galan-Rodriguez B (2005) Cannabinoid CB1 antagonists possess antiparkinsonian efficacy only in rats with severe nigral lesion in experimental parkinsonism. Neurobiol Dis 18:591–601

    Article  PubMed  CAS  Google Scholar 

  • Fernandez-Ruiz J (2009) The endocannabinoid system as a target for the treatment of motor dysfunction. Br J Pharmacol 156:1029–1040

    Article  PubMed  CAS  Google Scholar 

  • Fernandez-Ruiz J, Gonzales S (2005) Cannabinoid control of motor function at the basal ganglia. Handb Exp Pharmacol 168:479–507

    Google Scholar 

  • Ferreira SG, Teixeira FM, Garcao P, Agostinho P, Ledent C, Cortes L, Mackie K, Kofalvi A (2012) Presynaptic CB(1) cannabinoid receptors control frontocortical serotonin and glutamate release–species differences. Neurochem Int 61:219–226

    Article  PubMed  CAS  Google Scholar 

  • Ferrer B, Asbrock N, Kathuria S, Piomelli D, Giuffrida A (2003) Effects of levodopa on endocannabinoid levels in rat basal ganglia: implications for the treatment of levodopa-induced dyskinesias. Eur J Neurosci 18:1607–1614

    Article  PubMed  Google Scholar 

  • Fox SH, Henry B, Hill M, Crossman A, Brotchie J (2002) Stimulation of cannabinoid receptors reduces levodopa-induced dyskinesia in the MPTP-lesioned nonhuman primate model of Parkinson’s disease. Mov Disord 17:1180–1187

    Article  PubMed  Google Scholar 

  • Frankel JP, Hughes A, Lees AJ, Stern GM (1990) Marijuana for Parkinsonian tremor. J Neurol Neurosurg Psychiatry 53:436

    Article  PubMed  CAS  Google Scholar 

  • French ED, Dillon K, Wu X (1997) Cannabinoids excite dopamine neurons in the ventral tegmentum and substantia nigra. Neuroreport 8:649–652

    Article  PubMed  CAS  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 

  • Furmark T (2009) Neurobiological aspects of social anxiety disorder. Isr J Psychiatry Relat Sci 46:5–12

    PubMed  Google Scholar 

  • Galiègue S, Mary S, Marchand J, Dussossoy D, Carrière D, Carayon P, Bouaboula M, Shire D, Le Fur G, Casellas P (1995) Expression of central and peripheral cannabinoid receptors in human immune tissues and leukocyte subpopulations. Eur J Biochem 232:54–61

    Article  PubMed  Google Scholar 

  • Galve-Roperh I, Rueda D, Gomez del Pulgar T, Velasco G, Guzman M (2002) Mechanism of extracellular signal-regulated kinase activation by the CB(1) cannabinoid receptor. Mol Pharmacol 62:1385–1392

    Article  PubMed  CAS  Google Scholar 

  • Garcia C, Palomo-Garo C, Garcia-Arencibia M, Ramos J, Pertwee R, Fernandez-Ruiz J (2011) Symptom-relieving and neuroprotective effects of the phytocannabinoid Delta(9)-THCV in animal models of Parkinson’s disease. Br J Pharmacol 163:1495–1506

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Arencibia M, Garcia C, Fernandez-Ruiz J (2009) Cannabinoids and Parkinson’s disease. CNS Neurol Disord Drug Targets 8:432–439

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Arencibia M, Gonzalez S, Lago E de, Ramos JA, Mechoulam R, Fernandez-Ruiz J (2007) Evaluation of the neuroprotective effect of cannabinoids in a rat model of Parkinson’s disease: importance of antioxidant and cannabinoid receptor-independent properties. Brain Res 1134:162–170

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Gutierrez MS, Perez-Ortiz JM, Gutierrez-Adan A, Manzanares J (2010) Depression-resistant endophenotype in mice overexpressing cannabinoid CB(2) receptors. Br J Pharmacol 160:1773–1784

    Article  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 (1998a) Cannabinoids decrease acetylcholine release in the medial-prefrontal cortex and hippochampus, reversal by SR 141716A. Eur J Pharmacol 355:119–124

    Article  CAS  Google Scholar 

  • Gessa GL, Mascia MS, Casu MA, Carta G (1997) Inhibition of hippocampal acetylcholine release by cannabinoids: reversal by SR 141716A. Eur J Pharmacol 327:R1–R2

    Article  PubMed  CAS  Google Scholar 

  • Gessa GL, Melis M, Muntoni AL, Diana M (1998b) Cannabinoids activate mesolimbic dopamine neurons by an action on cannabinoid CB1 receptors. Eur J Pharmacol 341:39–44

    Article  CAS  Google Scholar 

  • Giuffrida A, Leweke FM, Gerth CW, Schreiber D, Koethe D, Faulhaber J, Klosterkotter J, Piomelli D (2004) Cerebrospinal anandamide levels are elevated in acute schizophrenia and are inversely correlated with psychotic symptoms. Neuropsychopharmacology 29:2108–2114

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Glass M, Dragunow M, Faull RL (1997) Cannabinoid receptors in the human brain: a detailed anatomical and quantitative autoradiographic study in the fetal, neonatal and adult human brain. Neuroscience 77:299–318

    Article  PubMed  CAS  Google Scholar 

  • Glass M, Felder CC (1997) Concurrent stimulation of cannabinoid CB1 and dopamine D2 receptors augments cAMP accumulation in striatal neurons: evidence for a Gs linkage to the CB1 receptor. J Neurosci 17:5327–5333

    PubMed  CAS  Google Scholar 

  • González S, Romero J, Miguel R de, Lastres-Becker I, Villanua MA, Makriyannis A, Ramos JA, Fernández-Ruiz JJ (1999) Extrapyramidal and neuroendocrine effects of AM404, an inhibitor of the carrier-mediated transport of anandamide. Life Sci 65:327–336

    Article  PubMed  Google Scholar 

  • Gonzalez S, Scorticati C, Garcia-Arencibia M, Miguel R de, Ramos JA, Fernandez-Ruiz J (2006) Effects of rimonabant, a selective cannabinoid CB1 receptor antagonist, in a rat model of Parkinson’s disease. Brain Res 1073–1074:209–219

    Google Scholar 

  • Gorriti MA, Rodriguez de Fonseca F, Navarro M, Palomo T (1999) Chronic (-)-delta9-tetrahydrocannabinol treatment induces sensitization to the psychomotor effects of amphetamine in rats. Eur J Pharmacol 365:133–142

    Article  PubMed  CAS  Google Scholar 

  • Green B, Kavanagh D, Young R (2003) Being stoned: a review of self-reported cannabis effects. Drug Alcohol Rev 22:453–460

    Article  PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Guidali C, Vigano D, Petrosino S, Zamberletti E, Realini N, Binelli G, Rubino T, Di Marzo V, Parolaro D (2011) Cannabinoid CB1 receptor antagonism prevents neurochemical and behavioural deficits induced by chronic phencyclidine. Int J Neuropsychopharmacol 14:17–28

    Article  PubMed  CAS  Google Scholar 

  • Haller J, Varga B, Ledent C, Barna I, Freund TF (2004) Context-dependent effects of CB1 cannabinoid gene disruption on anxiety-like and social behaviour in mice. Eur J Neurosci 19:1906–1912

    Article  PubMed  CAS  Google Scholar 

  • Haring M, Guggenhuber S, Lutz B (2012) Neuronal populations mediating the effects of endocannabinoids on stress and emotionality. Neuroscience 204:145–158

    Article  PubMed  CAS  Google Scholar 

  • Haring M, Marsicano G, Lutz B, Monory K (2007) Identification of the cannabinoid receptor type 1 in serotonergic cells of raphe nuclei in mice. Neuroscience 146:1212–1219

    Article  PubMed  CAS  Google Scholar 

  • Hayase T, Yamamoto Y, Yamamoto K (2005) Persistent anxiogenic effects of a single or repeated doses of cocaine and methamphetamine: interactions with endogenous cannabinoid receptor ligands. Behav Pharmacol 16:395–404

    Article  PubMed  CAS  Google Scholar 

  • Heifets BD, Castillo PE (2009) Endocannabinoid signaling and long-term synaptic plasticity. Annu Rev Physiol 71:283–306

    Article  PubMed  CAS  Google Scholar 

  • Henquet C, Murray R, Linszen D, Os J van (2005) The environment and schizophrenia: the role of cannabis use. Schizophr Bull 31:608–612

    Article  PubMed  Google Scholar 

  • Henstridge CM, Balenga NA, Kargl J, Andradas C, Brown AJ, Irving A, Sanchez C, Waldhoer M (2011) Minireview: recent developments in the physiology and pathology of the lysophosphatidylinositol-sensitive receptor GPR55. Mol Endocrinol 25:1835–1848

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Herkenham M, Lynn AB, Johnson MR, Melvin LS, Costa BR de, Rice KC (1991b) Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J Neurosci 11:563–583

    CAS  Google Scholar 

  • Herkenham M, Lynn AB, Little MD, Johnson MR, Melvin LS, Costa BR de, Rice KC (1990) Cannabinoid receptor localization in brain. Proc Natl Acad Sci U S A 87:1932–1936

    Article  PubMed  CAS  Google Scholar 

  • Hermann H, Marsicano G, Lutz B (2002) Coexpression of the cannabinoid receptor type 1 with dopamine and serotonin receptors in distinct neuronal subpopulations of the adult mouse forebrain. Neuroscience 109:451–460

    Article  PubMed  CAS  Google Scholar 

  • Hernandez-Tristan R, Arevalo C, Canals S, Leret ML (2000) The effects of acute treatment with delta9-THC on exploratory behaviour and memory in the rat. J Physiol Biochem 56:17–24

    Article  PubMed  CAS  Google Scholar 

  • Hojo M, Sudo Y, Ando Y, Minami K, Takada M, Matsubara T, Kanaide M, Taniyama K, Sumikawa K, Uezono Y (2008) mu-Opioid receptor forms a functional heterodimer with cannabinoid CB1 receptor: electrophysiological and FRET assay analysis. J Pharmacol Sci 108:308–319

    Article  PubMed  CAS  Google Scholar 

  • Howlett AC (2002) The cannabinoid receptors. Prostaglandins Other Lipid Mediat 68–69:619–631

    Google Scholar 

  • Howlett AC (2004) Efficacy in CB1 receptor-mediated signal transduction. Br J Pharmacol 142:1209–1218

    Article  PubMed  CAS  Google Scholar 

  • Hudson BD, Hebert TE, Kelly ME (2010a) Ligand- and heterodimer-directed signaling of the CB(1) cannabinoid receptor. Mol Pharmacol 77:1–9

    Article  CAS  Google Scholar 

  • Hudson BD, Hebert TE, Kelly ME (2010b) Physical and functional interaction between CB1 cannabinoid receptors and beta2-adrenoceptors. Br J Pharmacol 160:627–642

    Article  CAS  Google Scholar 

  • Huot P, Johnston TH, Koprich JB, Fox SH, Brotchie JM (2013) The pharmacology of L-dopa-induced dyskinesia in Parkinson’s disease. Pharmacol Rev 65:171–222

    PubMed  CAS  Google Scholar 

  • Hurley MJ, Mash DC, Jenner P (2003) Expression of cannabinoid CB1 receptor mRNA in basal ganglia of normal and parkinsonian human brain. J Neural Transm 110:1279–1288

    Article  PubMed  CAS  Google Scholar 

  • Iversen L (2005) Long-term effects of exposure to cannabis. Curr Opin Pharmacol 5:69–72

    Article  PubMed  CAS  Google Scholar 

  • Jarrahian A, Watts VJ, Barker EL (2004) D2 dopamine receptors modulate Galpha-subunit coupling of the CB1 cannabinoid receptor. J Pharmacol Exp Ther 308:880–886

    Article  PubMed  CAS  Google Scholar 

  • Jentsch JD, Elsworth JD, Taylor JR, Redmond DE Jr, Roth RH (1998) Dysregulation of mesoprefrontal dopamine neurons induced by acute and repeated phencyclidine administration in the nonhuman primate: implications for schizophrenia. Adv Pharmacol 42:810–814

    Article  PubMed  CAS  Google Scholar 

  • Jentsch JD, Tran A, Le D, Youngren KD, Roth RH (1997) Subchronic phencyclidine administration reduces mesoprefrontal dopamine utilization and impairs prefrontal cortical-dependent cognition in the rat. Neuropsychopharmacology 17:92–99

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kalant H (2004) Adverse effects of cannabis on health: an update of the literature since 1996. Prog Neuropsychopharmacol Biol Psychiatry 28:849–863

    Article  PubMed  CAS  Google Scholar 

  • Kano M, Ohno-Shosaku T, Hashimotodani Y, Uchigashima M, Watanabe M (2009) Endocannabinoid-mediated control of synaptic transmission. Physiol Rev 89:309–380

    Article  PubMed  CAS  Google Scholar 

  • 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 Schmiedebergs Arch Pharmacol 359:466–470

    Article  PubMed  CAS  Google Scholar 

  • Katona I, Freund TF (2012) Multiple functions of endocannabinoid signaling in the brain. Ann Rev Neurosci 35:529-58

    Google Scholar 

  • Katona I, Sperlagh B, Sik A, Kafalvi 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 

  • Kearn CS, Blake-Palmer K, Daniel E, Mackie K, Glass M (2005) Concurrent stimulation of cannabinoid CB1 and dopamine D2 receptors enhances heterodimer formation: a mechanism for receptor cross-talk? Mol Pharmacol 67:1697–1704

    Article  PubMed  CAS  Google Scholar 

  • Kelsey JE, Harris O, Cassin J (2009) The CB(1) antagonist rimonabant is adjunctively therapeutic as well as monotherapeutic in an animal model of Parkinson’s disease. Behav Brain Res 203:304–307

    Article  PubMed  CAS  Google Scholar 

  • Kleijn J, Wiskerke J, Cremers TI, Schoffelmeer AN, Westerink BH, Pattij T (2012) Effects of amphetamine on dopamine release in the rat nucleus accumbens shell region depend on cannabinoid CB1 receptor activation. Neurochem Int 60:791–798

    Article  PubMed  CAS  Google Scholar 

  • Koethe D, Giuffrida A, Schreiber D, Hellmich M, Schultze-Lutter F, Ruhrmann S, Klosterkotter J, Piomelli D, Leweke FM (2009a) Anandamide elevation in cerebrospinal fluid in initial prodromal states of psychosis. Br J Psychiatry 194:371–372

    Article  Google Scholar 

  • Koethe D, Hoyer C, Leweke FM (2009b) The endocannabinoid system as a target for modelling psychosis. Psychopharmacology (Berl) 206:551–561

    Article  CAS  Google Scholar 

  • Koethe D, Llenos IC, Dulay JR, Hoyer C, Torrey EF, Leweke FM, Weis S (2007) Expression of CB1 cannabinoid receptor in the anterior cingulate cortex in schizophrenia, bipolar disorder, and major depression. J Neural Transm 114:1055–1063

    Article  PubMed  CAS  Google Scholar 

  • Köfalvi A, Rodrigues RJ, Ledent C, Mackie K, Vizi ES, Cuhna 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

    Article  PubMed  CAS  Google Scholar 

  • Kortleven C, Fasano C, Thibault D, Lacaille JC, Trudeau LE (2011) The endocannabinoid 2-arachidonoylglycerol inhibits long-term potentiation of glutamatergic synapses onto ventral tegmental area dopamine neurons in mice. Eur J Neurosci 33:1751–1760

    Article  PubMed  Google Scholar 

  • Kreitzer AC, Malenka RC (2007) Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson’s disease models. Nature 445:643–647

    Article  PubMed  CAS  Google Scholar 

  • Laruelle M, Kegeles LS, Abi-Dargham A (2003a) Glutamate, dopamine, and schizophrenia: from pathophysiology to treatment. Ann N Y Acad Sci 1003:138–158

    Article  CAS  Google Scholar 

  • Laruelle M, Kegeles LS, Abi-Dargham A (2003b) Glutamate, dopamine, and schizophrenia: from pathophysiology to treatment. Ann N Y Acad Sci 1003:138–158

    Article  CAS  Google Scholar 

  • Lastres-Becker I, Cebeira M, Ceballos ML de, Zeng BY, Jenner P, Ramos JA, Fernandez-Ruiz JJ (2001) Increased cannabinoid CB1 receptor binding and activation of GTP-binding proteins in the basal ganglia of patients with Parkinson’s syndrome and of MPTP-treated marmosets. Eur J Neurosci 14:1827–1832

    Article  PubMed  CAS  Google Scholar 

  • Lastres-Becker I, Molina-Holgado E, Ramos JA, Mechoulam R, Fernandez-Ruiz J (2005) Cannabinoids provide neuroprotection against 6-hydroxydopamine toxicity in vivo and in vitro: relevance to Parkinson’s disease. Neurobiol Dis 19:96–107

    Article  PubMed  CAS  Google Scholar 

  • Lau T, Schloss P (2008) The cannabinoid CB1 receptor is expressed on serotonergic and dopaminergic neurons. Eur J Pharmacol 578:137–141

    Article  PubMed  CAS  Google Scholar 

  • Lauckner JE, Hille B, Mackie K (2005) The cannabinoid agonist WIN55,212–2 increases intracellular calcium via CB1 receptor coupling to Gq/11 G proteins. Proc Natl Acad Sci U S A 102:19144–19149

    Article  PubMed  CAS  Google Scholar 

  • Laviolette SR, Grace AA (2006) The roles of cannabinoid and dopamine receptor systems in neural emotional learning circuits: implications for schizophrenia and addiction. Cell Mol Life Sci 63:1597–1613

    Article  PubMed  CAS  Google Scholar 

  • Ledent C, Valverde O, Cossu G, Petitet F, Aubert JF, Beslot F, Bohme GA, Imperato A, Pedrazzini T, Roques BP, Vassart G, Fratta W, Parmentier M (1999) Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockout mice. Science 283:401–404

    Article  PubMed  CAS  Google Scholar 

  • Leweke FM, Giuffrida A, Koethe D, Schreiber D, Nolden BM, Kranaster L, Neatby MA, Schneider M, Gerth CW, Hellmich M, Klosterkotter J, Piomelli D (2007) Anandamide levels in cerebrospinal fluid of first-episode schizophrenic patients: impact of cannabis use. Schizophr Res 94:29–36

    Article  PubMed  Google Scholar 

  • Leweke FM, Giuffrida A, Wurster U, Emrich HM, Piomelli D (1999) Elevated endogenous cannabinoids in schizophrenia. Neuroreport 10:1665–1669

    Article  PubMed  CAS  Google Scholar 

  • Li X, Hoffman AF, Peng XQ, Lupica CR, Gardner EL, Xi ZX (2009) Attenuation of basal and cocaine-enhanced locomotion and nucleus accumbens dopamine in cannabinoid CB1-receptor-knockout mice. Psychopharmacology (Berl) 204:1–11

    Article  CAS  Google Scholar 

  • Lopez-Moreno JA, Gonzalez-Cuevas G, Moreno G, Navarro M (2008) The pharmacology of the endocannabinoid system: functional and structural interactions with other neurotransmitter systems and their repercussions in behavioral addiction. Addict Biol 13:160–187

    Article  PubMed  CAS  Google Scholar 

  • Lovinger DM, Mathur BN (2012) Endocannabinoids in striatal plasticity. Parkinsonism Relat Disord 18(Suppl 1):S132–134

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Mackie K (2005a) Cannabinoid receptor homo- and heterodimerization. Life Sci 77:1667–1673

    Article  CAS  Google Scholar 

  • Mackie K (2005b) Distribution of cannabinoid receptors in the central and peripheral nervous system. Handb Exp Pharmacol 299–325

    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 

  • Mailleux P, Parmentier M, Vanderhaeghen JJ (1992) Distribution of cannabinoid receptor messenger RNA in the human brain: an in situ hybridization histochemistry with oligonucleotides. Neurosci Lett 143:200–204

    Article  PubMed  CAS  Google Scholar 

  • Mailleux P, Vanderhaeghen JJ (1992a) 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  CAS  Google Scholar 

  • Mailleux P, Vanderhaeghen JJ (1992b) Localization of cannabinoid receptor in the human developing and adult basal ganglia. Higher levels in the striatonigral neurons. Neurosci Lett 148:173–176

    Article  CAS  Google Scholar 

  • Mailleux P, Vanderhaeghen JJ (1993) Dopaminergic regulation of cannabinoid receptor mRNA levels in the rat caudate-putamen: an in situ hybridization study. J Neurochem 61:1705–1712

    Article  PubMed  CAS  Google Scholar 

  • Malone DT, Taylor DA (1999) Modulation by fluoxetine of striatal dopamine release following Delta9-tetrahydrocannabinol: a microdialysis study in conscious rats. Br J Pharmacol 128:21–26

    Article  PubMed  CAS  Google Scholar 

  • Maneuf YP, Brotchie JM (1997) Paradoxical action of the cannabinoid WIN 55,212–2 in stimulated and basal cyclic AMP accumulation in rat globus pallidus slices. Br J Pharmacol 120:1397–1398

    Article  PubMed  CAS  Google Scholar 

  • Maneuf YP, Crossman AR, Brotchie JM (1997) The cannabinoid receptor agonist WIN 55,212–2 reduces D2, but not D1, dopamine receptor-mediated alleviation of akinesia in the reserpine-treated rat model of Parkinson’s disease. Exp Neurol 148:265–270

    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

    Google Scholar 

  • Marcellino D, Carriba P, Filip M, Borgkvist A, Frankowska M, Bellido I, Tanganelli S, Muller CE, Fisone G, Lluis C, Agnati LF, Franco R, Fuxe K (2008) Antagonistic cannabinoid CB1/dopamine D2 receptor interactions in striatal CB1/D2 heteromers. A combined neurochemical and behavioral analysis. Neuropharmacology 54:815–823

    Article  PubMed  CAS  Google Scholar 

  • Marinelli S, Di Marzo V, Berretta N, Matias I, Maccarrone M, Bernardi G, Mercuri NB (2003) Presynaptic facilitation of glutamatergic synapses to dopaminergic neurons of the rat substantia nigra by endogenous stimulation of vanilloid receptors. J Neurosci 23:3136–3144

    PubMed  CAS  Google Scholar 

  • Marinelli S, Di Marzo V, Florenzano F, Fezza F, Viscomi MT, Stelt M van der, Bernardi G, Molinari M, Maccarrone M, Mercuri NB (2007) N-arachidonoyl-dopamine tunes synaptic transmission onto dopaminergic neurons by activating both cannabinoid and vanilloid receptors. Neuropsychopharmacology 32:298–308

    Article  PubMed  CAS  Google Scholar 

  • Marsicano G, Lafenetre P (2009) Roles of the endocannabinoid system in learning and memory. Curr Top Behav Neurosci 1:201–230

    Article  PubMed  CAS  Google Scholar 

  • Marsicano G, Moosmann B, Hermann H, Lutz B, Behl C (2002) Neuroprotective properties of cannabinoids against oxidative stress: role of the cannabinoid receptor CB1. J Neurochem 80:448–456

    Article  PubMed  CAS  Google Scholar 

  • Martin AB, Fernandez-Espejo E, Ferrer B, Gorriti MA, Bilbao A, Navarro M, Rodriguez de Fonseca F, Moratalla R (2008) Expression and function of CB1 receptor in the rat striatum: localization and effects on D1 and D2 dopamine receptor-mediated motor behaviors. Neuropsychopharmacology 33:1667–1679

    Article  PubMed  CAS  Google Scholar 

  • Martinez A, Macheda T, Morgese MG, Trabace L, Giuffrida A (2012) The cannabinoid agonist WIN55212–2 decreases L-DOPA-induced PKA activation and dyskinetic behavior in 6-OHDA-treated rats. Neurosci Res 72:236–242

    Article  PubMed  CAS  Google Scholar 

  • Mathur BN, Lovinger DM (2012) Endocannabinoid-dopamine interactions in striatal synaptic plasticity. Front Pharmacol 3:66

    Article  PubMed  Google Scholar 

  • Matias I, Di Marzo V (2007) Endocannabinoids and the control of energy balance. Trends Endocrinol Metab 18:27–37

    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 

  • Matyas F, Yanovsky Y, Mackie K, Kelsch W, Misgeld U, Freund TF (2006) Subcellular localization of type 1 cannabinoid receptors in the rat basal ganglia. Neuroscience 137:337–361

    Article  PubMed  CAS  Google Scholar 

  • McIntosh BT, Hudson B, Yegorova S, Jollimore CA, Kelly ME (2007) Agonist-dependent cannabinoid receptor signalling in human trabecular meshwork cells. Br J Pharmacol 152:1111–1120

    Article  PubMed  CAS  Google Scholar 

  • McLaughlin RJ, Gobbi G (2012) Cannabinoids and emotionality: a neuroanatomical perspective. Neuroscience 204:134–144

    Article  PubMed  CAS  Google Scholar 

  • McPartland JM, Glass M, Pertwee RG (2007) Meta-analysis of cannabinoid ligand binding affinity and receptor distribution: interspecies differences. Br J Pharmacol 152:583–593

    Article  PubMed  CAS  Google Scholar 

  • Meador-Woodruff JH, Haroutunian V, Powchik P, Davidson M, Davis KL, Watson SJ (1997) Dopamine receptor transcript expression in striatum and prefrontal and occipital cortex. Focal abnormalities in orbitofrontal cortex in schizophrenia. Arch Gen Psychiatry 54:1089–1095

    Article  PubMed  CAS  Google Scholar 

  • Meijerink J, Balvers M, Witkamp R (2012) N-acyl amines of docosahexaenoic acid and other n-3 polyunsatured fatty acids—From fishy endocannabinoids to potential leads. Br J Pharmacol 169(4):772–83 (2013 Jun)

    Google Scholar 

  • Melis M, Gessa GL, Diana M (2000) Different mechanisms for dopaminergic excitation induced by opiates and cannabinoids in the rat midbrain. Prog Neuro-Psychopharmacol Biol Psychiatry 24:993–1006

    Article  CAS  Google Scholar 

  • Melis M, Perra S, Muntoni AL, Pillolla G, Lutz B, Marsicano G, Di Marzo V, Gessa GL, Pistis M (2004a) Prefrontal cortex stimulation induces 2-arachidonoyl-glycerol-mediated suppression of excitation in dopamine neurons. J Neurosci 24:10707–10715

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Melis M, Pistis P (2007) Endocannabinoid signaling in midbrain dopamine neurons: more than physiology? Curr Neuropharmacol 5:268–277

    Article  PubMed  CAS  Google Scholar 

  • Meltzer HY, Arvanitis L, Bauer D, Rein W (2004) Placebo-controlled evaluation of four novel compounds for the treatment of schizophrenia and schizoaffective disorder. Am J Psychiatry 161:975–984

    Article  PubMed  Google Scholar 

  • Meschler JP, Howlett AC (2001) Signal transduction interactions between CB1 cannabinoid and dopamine receptors in the rat and monkey striatum. Neuropharmacology 40:918–926

    Article  PubMed  CAS  Google Scholar 

  • Meschler JP, Howlett AC, Madras BK (2001) Cannabinoid receptor agonist and antagonist effects on motor function in normal and 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine (MPTP)-treated non-human primates. Psychopharmacology (Berl) 156:79–85

    Article  CAS  Google Scholar 

  • Mesnage V, Houeto JL, Bonnet AM, Clavier I, Arnulf I, Cattelin F, Le Fur G, Damier P, Welter ML, Agid Y (2004) Neurokinin B, neurotensin, and cannabinoid receptor antagonists and Parkinson disease. Clin Neuropharmacol 27:108–110

    Article  PubMed  CAS  Google Scholar 

  • Missale C, Nash SR, Robinson SW, Jaber M, Caron MG (1998) Dopamine receptors: from structure to function. Physiol Rev 78:189–225

    PubMed  CAS  Google Scholar 

  • Moldrich G, Wenger T (2000) Localization of the CB1 cannabinoid receptor in the rat brain. An immunohistochemical study. Peptides 21:1735–1742

    Article  PubMed  CAS  Google Scholar 

  • Moranta D, Esteban S, Garcia-Sevilla JA (2004) Differential effects of acute cannabinoid drug treatment, mediated by CB1 receptors, on the in vivo activity of tyrosine and tryptophan hydroxylase in the rat brain. Naunyn Schmiedebergs Arch Pharmacol 369:516–524

    Article  PubMed  CAS  Google Scholar 

  • Moranta D, Esteban S, Garcia-Sevilla JA (2009) Chronic treatment and withdrawal of the cannabinoid agonist WIN 55,212–2 modulate the sensitivity of presynaptic receptors involved in the regulation of monoamine syntheses in rat brain. Naunyn Schmiedebergs Arch Pharmacol 379:61–72

    Article  PubMed  CAS  Google Scholar 

  • Morera-Herreras T, Miguelez C, Aristieta A, Ruiz-Ortega JA, Ugedo L (2012) Endocannabinoid modulation of dopaminergic motor circuits. Front Pharmacol 3:110

    Article  PubMed  CAS  Google Scholar 

  • Morgese MG, Cassano T, Cuomo V, Giuffrida A (2007) Anti-dyskinetic effects of cannabinoids in a rat model of Parkinson’s disease: role of CB(1) and TRPV1 receptors. Exp Neurol 208:110–119

    Article  PubMed  CAS  Google Scholar 

  • Muller-Vahl KR, Emrich HM (2008) Cannabis and schizophrenia: towards a cannabinoid hypothesis of schizophrenia. Expert Rev Neurother 8:1037–1048

    Article  PubMed  Google Scholar 

  • Munro S, Thomas KL, Abu-Shaar M (1993) Molecular characterization of a peripheral receptor for cannabinoids. Nature 365:61–65

    Article  PubMed  CAS  Google Scholar 

  • Nakazi M, Bauer U, Nickel T, Kathmann M, Schlicker E (2000) Inhibition of serotonin release in the mouse brain via presynaptic cannabinoid CB1 receptors. Naunyn Schmiedebergs Arch Pharmacol 361:19–24

    Article  PubMed  CAS  Google Scholar 

  • Nasehi M, Sahebgharani M, Haeri-Rohani A, Zarrindast MR (2009) Effects of cannabinoids infused into the dorsal hippocampus upon memory formation in 3-days apomorphine-treated rats. Neurobiol Learn Mem 92:391–399

    Article  PubMed  CAS  Google Scholar 

  • Nava F, Carta G, Battasi AM, Gessa GL (2000) D(2) dopamine receptors enable delta(9)-tetrahydrocannabinol induced memory impairment and reduction of hippocampal extracellular acetylcholine concentration. Br J Pharmacol 130:1201–1210

    Article  PubMed  CAS  Google Scholar 

  • Navarro G, Carriba P, Gandia J, Ciruela F, Casado V, Cortes A, Mallol J, Canela EI, Lluis C, Franco R (2008) Detection of heteromers formed by cannabinoid CB1, dopamine D2, and adenosine A2A G-protein-coupled receptors by combining bimolecular fluorescence complementation and bioluminescence energy transfer. ScientificWorldJournal 8:1088–1097

    Article  PubMed  CAS  Google Scholar 

  • Newell KA, Deng C, Huang XF (2006) Increased cannabinoid receptor density in the posterior cingulate cortex in schizophrenia. Exp Brain Res 172:556–560

    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 

  • Nissen SE, Nicholls SJ, Wolski K, Rodes-Cabau J, Cannon CP, Deanfield JE, Despres JP, Kastelein JJ, Steinhubl SR, Kapadia S, Yasin M, Ruzyllo W, Gaudin C, Job B, Hu B, Bhatt DL, Lincoff AM, Tuzcu EM (2008) Effect of rimonabant on progression of atherosclerosis in patients with abdominal obesity and coronary artery disease: the STRADIVARIUS randomized controlled trial. JAMA 299:1547–1560

    Article  PubMed  CAS  Google Scholar 

  • Nunez E, Benito C, Pazos MR, Barbachano A, Fajardo O, Gonzalez S, Tolon RM, Romero J (2004) Cannabinoid CB2 receptors are expressed by perivascular microglial cells in the human brain: an immunohistochemical study. Synapse 53:208–213

    Article  PubMed  CAS  Google Scholar 

  • Obeso JA, Rodriguez-Oroz MC, Benitez-Temino B, Blesa FJ, Guridi J, Marin C, Rodriguez M (2008) Functional organization of the basal ganglia: therapeutic implications for Parkinson’s disease. Mov Disord 23(Suppl 3):S548–S559

    Article  PubMed  Google Scholar 

  • Onaivi ES (2006) Neuropsychobiological evidence for the functional presence and expression of cannabinoid CB2 receptors in the brain. NeuropsychoBiology 54:231–246

    Article  PubMed  CAS  Google Scholar 

  • Onaivi ES, Ishiguro H, Gong JP, Patel S, Perchuk A, Meozzi PA, Myers L, Mora Z, Tagliaferro P, Gardner E, Brusco A, Akinshola BE, Liu QR, Hope B, Iwasaki S, Arinami T, Teasenfitz L, Uhl GR (2006) Discovery of the presence and functional expression of cannabinoid CB2 receptors in brain. Ann N Y Acad Sci 1074:514–536

    Article  PubMed  CAS  Google Scholar 

  • Onaivi ES, Ishiguro H, Gu S, Liu QR (2011) CNS effects of CB2 cannabinoid receptors: beyond neuro-immuno-cannabinoid activity. J Psychopharmacol 26(1):92-103

    Google Scholar 

  • Oropeza VC, Mackie K, Van Bockstaele EJ (2007) Cannabinoid receptors are localized to noradrenergic axon terminals in the rat frontal cortex. Brain Res 1127:36–44

    Article  PubMed  CAS  Google Scholar 

  • Pan B, Hillard CJ, Liu QS (2008) D2 dopamine receptor activation facilitates endocannabinoid-mediated long-term synaptic depression of GABAergic synaptic transmission in midbrain dopamine neurons via cAMP-protein kinase A signaling. J Neurosci 28:14018–14030

    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 

  • Pandey R, Mousawy K, Nagarkatti M, Nagarkatti P (2009) Endocannabinoids and immune regulation. Pharmacol Res 60:85–92

    Article  PubMed  CAS  Google Scholar 

  • Parolaro D, Rubino T (2008) The role of the endogenous cannabinoid system in drug addiction. Drug News Perspect 21:149–157

    PubMed  CAS  Google Scholar 

  • Patel KD, Davison JS, Pittman QJ, Sharkey KA (2010) Cannabinoid CB(2) receptors in health and disease. Curr Med Chem 17:1393–1410

    Article  PubMed  Google Scholar 

  • Patel S, Rademacher DJ, Hillard CJ (2003) Differential regulation of the endocannabinoids anandamide and 2-arachidonylglycerol within the limbic forebrain by dopamine receptor activity. J Pharmacol Exp Ther 306:880–888

    Article  PubMed  CAS  Google Scholar 

  • Pazos MR, Nunez E, Benito C, Tolon RM, Romero J (2005) Functional neuroanatomy of the endocannabinoid system. Pharmacol Biochem Behav 81:239–247

    Article  PubMed  CAS  Google Scholar 

  • Perez-Rial S, Garcia-Gutierrez MS, Molina JA, Perez-Nievas BG, Ledent C, Leiva C, Leza JC, Manzanares J (2011) Increased vulnerability to 6-hydroxydopamine lesion and reduced development of dyskinesias in mice lacking CB1 cannabinoid receptors. Neurobiol Aging 32:631–645

    Article  PubMed  CAS  Google Scholar 

  • Pertwee RG (2006) The pharmacology of cannabinoid receptors and their ligands: an overview. Int J Obes (Lond) 30(Suppl 1):S13–18

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Piomelli D (2003) The molecular logic of endocannabinoid signalling. Nat Rev Neurosci 4:873–884

    Article  PubMed  CAS  Google Scholar 

  • Pisani A, Fezza F, Galati S, Battista N, Napolitano S, Finazzi-Agro A, Bernardi G, Brusa L, Pierantozzi M, Stanzione P, Maccarrone M (2005) High endogenous cannabinoid levels in the cerebrospinal fluid of untreated Parkinson’s disease patients. Ann Neurol 57:777–779

    Article  PubMed  Google Scholar 

  • Pisani V, Madeo G, Tassone A, Sciamanna G, Maccarrone M, Stanzione P, Pisani A (2011) Homeostatic changes of the endocannabinoid system in Parkinson’s disease. Mov Disord 26:216–222

    Article  PubMed  Google Scholar 

  • Pistis M, Ferraro L, Pira L, Flore G, Tanganelli S, Gessa GL, Devoto P (2002) Delta(9)-tetrahydrocannabinol decreases extracellular GABA and increases extracellular glutamate and dopamine levels in the rat prefrontal cortex: an in vivo microdialysis study. Brain Res 948:155–158

    Article  PubMed  CAS  Google Scholar 

  • Pistis M, Porcu G, Melis M, Diana M, Gessa GL (2001) Effects of cannabinoids on prefrontal neuronal responses to ventral tegmental area stimulation. Eur J Neurosci 14:96–102

    Article  PubMed  CAS  Google Scholar 

  • Pivonello R, Ferone D, Lombardi G, Colao A, Lamberts SW, Hofland LJ (2007) Novel insights in dopamine receptor physiology. Eur J Endocrinol 156(Suppl 1):S13–S21

    Article  PubMed  CAS  Google Scholar 

  • Polissidis A, Galanopoulos A, Naxakis G, Papahatjis D, Papadopoulou-Daifoti Z, Antoniou K (2012) The cannabinoid CB1 receptor biphasically modulates motor activity and regulates dopamine and glutamate release region dependently. Int J Neuropsychopharmacol 1–11

    Google Scholar 

  • Prescott WR, Gold LH, Martin BR (1992) Evidence for separate neuronal mechanisms for the discriminative stimulus and catalepsy induced by delta 9-THC in the rat. Psychopharmacology (Berl) 107:117–124

    Article  CAS  Google Scholar 

  • Price DA, Martinez AA, Seillier A, Koek W, Acosta Y, Fernandez E, Strong R, Lutz B, Marsicano G, Roberts JL, Giuffrida A (2009) WIN55,212–2, a cannabinoid receptor agonist, protects against nigrostriatal cell loss in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson’s disease. Eur J Neurosci 29:2177–2186

    Article  PubMed  Google Scholar 

  • Ranganathan M, D’Souza DC (2006) The acute effects of cannabinoids on memory in humans: a review. Psychopharmacology (Berl) 188:425–444

    Article  CAS  Google Scholar 

  • Reilly D, Didcott P, Swift W, Hall W (1998) Long-term cannabis use: characteristics of users in an Australian rural area. Addiction 93:837–846

    Article  PubMed  CAS  Google Scholar 

  • Rhee MH, Nevo I, Avidor-Reiss T, Levy R, Vogel Z (2000) Differential superactivation of adenylyl cyclase isozymes after chronic activation of the CB(1) cannabinoid receptor. Mol Pharmacol 57:746–752

    PubMed  CAS  Google Scholar 

  • Riegel AC, Lupica CR (2004) Independent presynaptic and postsynaptic mechanisms regulate endocannabinoid signaling at multiple synapses in the ventral tegmental area. J Neurosci 24:11070–11078

    Article  PubMed  CAS  Google Scholar 

  • Rios C, Gomes I, Devi LA (2006) mu opioid and CB1 cannabinoid receptor interactions: reciprocal inhibition of receptor signaling and neuritogenesis. Br J Pharmacol 148:387–395

    Article  PubMed  CAS  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 

  • Robinson HM, Hood SD, Bell CJ, Nutt DJ (2006) Dopamine and social anxiety disorder. Rev Bras Psiquiatr 28:263–264

    Article  PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Romero J, Berrendero F, Perez-Rosado A, Manzanares J, Rojo A, Fernandez-Ruiz JJ, Yebenes JG de, Ramos JA (2000) Unilateral 6-hydroxydopamine lesions of nigrostriatal dopaminergic neurons increased CB1 receptor mRNA levels in the caudate-putamen. Life Sci 66:485–494

    Article  PubMed  CAS  Google Scholar 

  • Rubino T, Realini N, Castiglioni C, Guidali C, Vigano D, Marras E, Petrosino S, Perletti G, Maccarrone M, Di Marzo V, Parolaro D (2008) Role in anxiety behavior of the endocannabinoid system in the prefrontal cortex. Cereb Cortex 18:1292–1301

    Article  PubMed  CAS  Google Scholar 

  • Rueda D, Galve-Roperh I, Haro A, Guzman M (2000) The CB(1) cannabinoid receptor is coupled to the activation of c-Jun N-terminal kinase. Mol Pharmacol 58:814–820

    PubMed  CAS  Google Scholar 

  • Ruehle S, Rey AA, Remmers F, Lutz B (2012) The endocannabinoid system in anxiety, fear memory and habituation. J Psychopharmacol 26:23–39

    Article  PubMed  CAS  Google Scholar 

  • San L, Bernardo M, Gomez A, Pena M (2012) Factors associated with relapse in patients with schizophrenia. Int J Psychiatry Clin Pract 17(1):2-9

    Google Scholar 

  • Sanudo-Pena MC, Patrick SL, Khen S, Patrick RL, Tsou K, Walker JM (1998) Cannabinoid effects in basal ganglia in a rat model of Parkinson’s disease. Neurosci Lett 248:171–174

    Article  PubMed  CAS  Google Scholar 

  • Schatz AR, Lee M, Condie RB, Pulaski JT, Kaminski NE (1997) Cannabinoid receptors CB1 and CB2: a characterization of expression and adenylate cyclase modulation within the immune system. Toxicol Appl Pharmacol 142:278–287

    Article  PubMed  CAS  Google Scholar 

  • Schneier FR, Abi-Dargham A, Martinez D, Slifstein M, Hwang DR, Liebowitz MR, Laruelle M (2009) Dopamine transporters, D2 receptors, and dopamine release in generalized social anxiety disorder. Depress Anxiety 26:411–418

    Article  PubMed  CAS  Google Scholar 

  • Schneier FR, Liebowitz MR, Abi-Dargham A, Zea-Ponce Y, Lin SH, Laruelle M (2000) Low dopamine D(2) receptor binding potential in social phobia. Am J Psychiatry 157:457–459

    Article  PubMed  CAS  Google Scholar 

  • Schneier FR, Martinez D, Abi-Dargham A, Zea-Ponce Y, Simpson HB, Liebowitz MR, Laruelle M (2008) Striatal dopamine D(2) receptor availability in OCD with and without comorbid social anxiety disorder: preliminary findings. Depress Anxiety 25:1–7

    Article  PubMed  Google Scholar 

  • Seillier A, Advani T, Cassano T, Hensler JG, Giuffrida A (2010) Inhibition of fatty-acid amide hydrolase and CB1 receptor antagonism differentially affect behavioural responses in normal and PCP-treated rats. Int J Neuropsychopharmacol 13:373–386

    Article  PubMed  CAS  Google Scholar 

  • Sewell RA, Ranganathan M, D’Souza DC (2009) Cannabinoids and psychosis. Int Rev Psychiatry 21:152–162

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Sieradzan KA, Fox SH, Hill M, Dick JP, Crossman AR, Brotchie JM (2001) Cannabinoids reduce levodopa-induced dyskinesia in Parkinson’s disease: a pilot study. Neurology 57:2108–2111

    Article  PubMed  CAS  Google Scholar 

  • Silverdale MA, McGuire S, McInnes A, Crossman AR, Brotchie JM (2001) Striatal cannabinoid CB1 receptor mRNA expression is decreased in the reserpine-treated rat model of Parkinson’s disease. Exp Neurol 169:400–406

    Article  PubMed  CAS  Google Scholar 

  • Solinas M, Justinova Z, Goldberg SR, Tanda G (2006) Anandamide administration alone and after inhibition of fatty acid amide hydrolase (FAAH) increases dopamine levels in the nucleus accumbens shell in rats. J Neurochem 98:408–419

    Article  PubMed  CAS  Google Scholar 

  • Spano MS, Fadda P, Frau R, Fattore L, Fratta W (2010) Cannabinoid self-administration attenuates PCP-induced schizophrenia-like symptoms in adult rats. Eur Neuropsychopharmacol 20:25–36

    Article  PubMed  CAS  Google Scholar 

  • Stefanis NC, Bresnick JN, Kerwin RW, Schofield WN, McAllister G (1998) Elevation of D4 dopamine receptor mRNA in postmortem schizophrenic brain. Brain Res Mol Brain Res 53:112–119

    Article  PubMed  CAS  Google Scholar 

  • Steffens M, Engler C, Zentner J, Feuerstein TJ (2004) Cannabinoid CB1 receptor-mediated modulation of evoked dopamine release and of adenylyl cyclase activity in the human neocortex. Br J Pharmacol 141:1193–1203

    Article  PubMed  CAS  Google Scholar 

  • Stella N (2010) Cannabinoid and cannabinoid-like receptors in microglia, astrocytes, and astrocytomas. Glia 58:1017–1030

    Article  PubMed  Google Scholar 

  • Suarez J, Llorente R, Romero-Zerbo SY, Mateos B, Bermudez-Silva FJ, Fonseca FR de, Viveros MP (2009) Early maternal deprivation induces gender-dependent changes on the expression of hippocampal CB(1) and CB(2) cannabinoid receptors of neonatal rats. Hippocampus 19:623–632

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  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, 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 

  • Szuster RR, Pontius EB, Campos PE (1988) Marijuana sensitivity and panic anxiety. J Clin Psychiatry 49:427–429

    PubMed  CAS  Google Scholar 

  • Tambaro S, Bortolato M (2012) Cannabinoid-related agents in the treatment of anxiety disorders: current knowledge and future perspectives. Recent Pat CNS Drug Discov 7:25–40

    Article  PubMed  CAS  Google Scholar 

  • Tanda G, Pontieri FE, Di Chiara G (1997) Cannabinoid and heroin activation of mesolimbic dopamine transmission by a common mu1 opioid receptor mechanism. Science 276:2048–2050

    Article  PubMed  CAS  Google Scholar 

  • Terzian AL, Drago F, Wotjak CT, Micale V (2011) The dopamine and cannabinoid interaction in the modulation of emotions and cognition: assessing the role of cannabinoid CB1 receptor in neurons expressing dopamine D1 receptors. Front Behav Neurosci 5:49

    Article  PubMed  CAS  Google Scholar 

  • Thiemann G, Di Marzo V, Molleman A, Hasenohrl RU (2008) The CB(1) cannabinoid receptor antagonist AM251 attenuates amphetamine-induced behavioural sensitization while causing monoamine changes in nucleus accumbens and hippocampus. Pharmacol Biochem Behav 89:384–391

    Article  PubMed  CAS  Google Scholar 

  • Thiemann G, Watt CA, Ledent C, Molleman A, Hasenohrl RU (2009) Modulation of anxiety by acute blockade and genetic deletion of the CB(1) cannabinoid receptor in mice together with biogenic amine changes in the forebrain. Behav Brain Res 200:60–67

    Article  PubMed  CAS  Google Scholar 

  • Toda M, Abi-Dargham A (2007) Dopamine hypothesis of schizophrenia: making sense of it all. Curr Psychiatry Rep 9:329–336

    Article  PubMed  Google Scholar 

  • Trezza V, Damsteegt R, Manduca A, Petrosino S, Van Kerkhof LW, Pasterkamp RJ, Zhou Y, Campolongo P, Cuomo V, Di Marzo V, Vanderschuren LJ (2012) Endocannabinoids in amygdala and nucleus accumbens mediate social play reward in adolescent rats. J Neurosci 32:14899–14908

    Article  PubMed  CAS  Google Scholar 

  • Trezza V, Vanderschuren LJ (2009) Divergent effects of anandamide transporter inhibitors with different target selectivity on social play behavior in adolescent rats. J Pharmacol Exp Ther 328:343–350

    Article  PubMed  CAS  Google Scholar 

  • Tsou K, Nogueron MI, Muthian S, Sanudo-Pena MC, Hillard CJ, Deutsch DG, Walker JM (1998) Fatty acid amide hydrolase is located preferentially in large neurons in the rat central nervous system as revealed by immunohistochemistry. Neurosci Lett 254:137–140

    Article  PubMed  CAS  Google Scholar 

  • Turu G, Hunyady L (2010) Signal transduction of the CB1 cannabinoid receptor. J Mol Endocrinol 44:75–85

    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, Davis RJ, Perry KW, Li X, Salhoff C, Bymaster FP, Witkin JM, Nomikos GG (2003) 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, Li DL, Moutsimilli L, Bisogno T, Di Marzo V, Phebus LA, Nomikos GG, Giros B (2006) Endocannabinoids activate transient receptor potential vanilloid 1 receptors to reduce hyperdopaminergia-related hyperactivity: therapeutic implications. Biol Psychiatry 59:508–515

    Article  PubMed  CAS  Google Scholar 

  • Ujike H, Morita Y (2004) New perspectives in the studies on endocannabinoid and cannabis: cannabinoid receptors and schizophrenia. J Pharmacol Sci 96:376–381

    Article  PubMed  CAS  Google Scholar 

  • Umathe SN, Manna SS, Utturwar KS, Jain NS (2009) Endocannabinoids mediate anxiolytic-like effect of acetaminophen via CB1 receptors. Prog Neuropsychopharmacol Biol Psychiatry 33:1191–1199

    Article  PubMed  CAS  Google Scholar 

  • Uriguen L, Garcia-Fuster MJ, Callado LF, Morentin B, La Harpe R, Casado V, Lluis C, Franco R, Garcia-Sevilla JA, Meana JJ (2009) Immunodensity and mRNA expression of A2A adenosine, D2 dopamine, and CB1 cannabinoid receptors in postmortem frontal cortex of subjects with schizophrenia: effect of antipsychotic treatment. Psychopharmacology (Berl) 206:313–324

    Article  CAS  Google Scholar 

  • Uriguen L, Perez-Rial S, Ledent C, Palomo T, Manzanares J (2004) Impaired action of anxiolytic drugs in mice deficient in cannabinoid CB1 receptors. Neuropharmacology 46:966–973

    Article  PubMed  CAS  Google Scholar 

  • Stelt M van der, Di Marzo V (2003) The endocannabinoid system in the basal ganglia and in the mesolimbic reward system: implications for neurological and psychiatric disorders. Eur J Pharmacol 480:133–150

    Article  PubMed  CAS  Google Scholar 

  • Stelt M van der, Fox SH, Hill M, Crossman AR, Petrosino S, Di Marzo V, Brotchie JM (2005) A role for endocannabinoids in the generation of parkinsonism and levodopa-induced dyskinesia in MPTP-lesioned non-human primate models of Parkinson’s disease. FASEB J 19:1140–1142

    PubMed  Google Scholar 

  • Stelt M van der, Veldhuis WB, Maccarrone M, Bar PR, Nicolay K, Veldink GA, Di Marzo V, Vliegenthart JF (2002) Acute neuronal injury, excitotoxicity, and the endocannabinoid system. Mol Neurobiol 26:317–346

    Article  PubMed  Google Scholar 

  • Van Laere K, Casteels C, Lunskens S, Goffin K, Grachev ID, Bormans G, Vandenberghe W (2012) Regional changes in type 1 cannabinoid receptor availability in Parkinson’s disease in vivo. Neurobiol Aging 33:620 e 621–628

    Article  CAS  Google Scholar 

  • Os J van, Kapur S (2009) Schizophrenia. Lancet 374:635–645

    Article  PubMed  CAS  Google Scholar 

  • Van Sickle MD, Duncan M, Kingsley PJ, Mouihate A, Urbani P, Mackie K, Stella N, Makriyannis A, Piomelli D, Davison JS, Marnett LJ, Di Marzo V, Pittman QJ, Patel KD, Sharkey KA (2005) Identification and functional characterization of brainstem cannabinoid CB2 receptors. Science 310:329–332

    Article  PubMed  CAS  Google Scholar 

  • Vliet SA van, Vanwersch RA, Jongsma MJ, Olivier B, Philippens IH (2008) Therapeutic effects of Delta9-THC and modafinil in a marmoset Parkinson model. Eur Neuropsychopharmacol 18:383–389

    Article  PubMed  CAS  Google Scholar 

  • Vasquez C, Navarro-Polanco RA, Huerta M, Trujillo X, Andrade F, Trujillo-Hernandez B, Hernandez L (2003) Effects of cannabinoids on endogenous K + and Ca2 + currents in HEK293 cells. Can J Physiol Pharmacol 81:436–442

    Article  PubMed  CAS  Google Scholar 

  • Vigano D, Guidali C, Petrosino S, Realini N, Rubino T, Di Marzo V, Parolaro D (2009) Involvement of the endocannabinoid system in phencyclidine-induced cognitive deficits modelling schizophrenia. Int J Neuropsychopharmacol 12:599–614

    Article  PubMed  CAS  Google Scholar 

  • Wager-Miller J, Westenbroek R, Mackie K (2002) Dimerization of G protein-coupled receptors: CB1 cannabinoid receptors as an example. Chem Phys Lipids 121:83–89

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Walsh S, Gorman AM, Finn DP, Dowd E (2010) The effects of cannabinoid drugs on abnormal involuntary movements in dyskinetic and non-dyskinetic 6-hydroxydopamine lesioned rats. Brain Res 1363:40–48

    Article  PubMed  CAS  Google Scholar 

  • Wei BQ, Mikkelsen TS, McKinney MK, Lander ES, Cravatt BF (2006) A second fatty acid amide hydrolase with variable distribution among placental mammals. J Biol Chem 281:36569–36578

    Article  PubMed  CAS  Google Scholar 

  • Wenger T, Moldrich G, Furst S (2003) Neuromorphological background of cannabis addiction. Brain Res Bull 61:125–128

    Article  PubMed  CAS  Google Scholar 

  • Wong DF, Kuwabara H, Horti AG, Raymont V, Brasic J, Guevara M, Ye W, Dannals RF, Ravert HT, Nandi A, Rahmim A, Ming JE, Grachev I, Roy C, Cascella N (2010) Quantification of cerebral cannabinoid receptors subtype 1 (CB1) in healthy subjects and schizophrenia by the novel PET radioligand [11C]OMAR. Neuroimage 52:1505–1513

    Article  PubMed  CAS  Google Scholar 

  • Wotjak CT (2005) Role of endogenous cannabinoids in cognition and emotionality. Mini Rev Med Chem 5:659–670

    Article  PubMed  CAS  Google Scholar 

  • Wu X, French ED (2000) Effects of chronic delta9-tetrahydrocannabinol on rat midbrain dopamine neurons: an electrophysiological assessment. Neuropharmacology 39:391–398

    Article  PubMed  CAS  Google Scholar 

  • Zarrindast MR, Dorrani M, Lachinani R, Rezayof A (2010) Blockade of dorsal hippocampal dopamine receptors inhibits state-dependent learning induced by cannabinoid receptor agonist in mice. Neurosci Res 67:25–32

    Article  PubMed  CAS  Google Scholar 

  • Zarrindast MR, Mahboobi S, Sadat-Shirazi MS, Ahmadi S (2011a) Anxiolytic-like effect induced by the cannabinoid CB1 receptor agonist, arachydonilcyclopropylamide (ACPA), in the rat amygdala is mediated through the D1 and D2 dopaminergic systems. J Psychopharmacol 25:131–140

    Article  CAS  Google Scholar 

  • Zarrindast MR, Navaeian M, Nasehi M (2011b) Influence of three-day morphine-treatment upon impairment of memory consolidation induced by cannabinoid infused into the dorsal hippocampus in rats. Neurosci Res 69:51–59

    Article  CAS  Google Scholar 

  • Zavitsanou K, Garrick T, Huang XF (2004) Selective antagonist [3H]SR141716A binding to cannabinoid CB1 receptors is increased in the anterior cingulate cortex in schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 28:355–360

    Article  PubMed  CAS  Google Scholar 

  • Zeng BY, Dass B, Owen A, Rose S, Cannizzaro C, Tel BC, Jenner P (1999) Chronic L-DOPA treatment increases striatal cannabinoid CB1 receptor mRNA expression in 6-hydroxydopamine-lesioned rats. Neurosci Lett 276:71–74

    Article  PubMed  CAS  Google Scholar 

  • Zenko M, Zhu Y, Dremencov E, Ren W, Xu L, Zhang X (2011) Requirement for the endocannabinoid system in social interaction impairment induced by coactivation of dopamine D1 and D2 receptors in the piriform cortex. J Neurosci Res 89:1245–1258

    Article  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 96:5780–5785

    Article  PubMed  CAS  Google Scholar 

  • Zuardi AW, Guimaraes FS, Hallak JE, Crippa JA (2011) Is the highest density of CB1 receptors in paranoid schizophrenia a correlate of endocannabinoid system functioning? Expert Rev Neurother 11:1111–1114

    Article  PubMed  CAS  Google Scholar 

Download references

Conflict of Interest

We declare no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Pharmacology, UT Health Science Center San Antonio, 7703 Floyd Curl Drive, 78229-3900, San Antonio, TX, USA

    Julien Matricon & Andrea Giuffrida PhD

Authors
  1. Julien Matricon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrea Giuffrida PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrea Giuffrida PhD .

Editor information

Editors and Affiliations

  1. , Department of Neuroscience, Thomas Jefferson University, Walnut Street 900, Philadelphia, 19147, Pennsylvania, USA

    Elisabeth J. Van Bockstaele

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media New York

About this chapter

Cite this chapter

Matricon, J., Giuffrida, A. (2013). Cannabinoid Modulation of Dopaminergic Circuits in Neurodegenerative and Neuropsychiatric Disorders. In: Van Bockstaele, E. (eds) Endocannabinoid Regulation of Monoamines in Psychiatric and Neurological Disorders. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-7940-6_5

Download citation

Publish with us

Policies and ethics

Search

Navigation