Abstract
Marijuana and its psychoactive constituents induce a multitude of effects on brain function. These include deficits in memory formation, but care needs to be exercised since many human studies are flawed by multiple drug abuse, small sample sizes, sample selection and sensitivity of psychological tests for subtle differences. The most robust finding with respect to memory is a deficit in working and short-term memory. This requires intact hippocampus and prefrontal cortex, two brain regions richly expressing CB1 receptors. Animal studies, which enable a more controlled drug regime and more constant behavioural testing, have confirmed human results and suggest, with respect to hippocampus, that exogenous cannabinoid treatment selectively affects encoding processes. This may be different in other brain areas, for instance the amygdala, where a predominant involvement in memory consolidation and forgetting has been firmly established. While cannabinoid receptor agonists impair memory formation, antagonists reverse these deficits or act as memory enhancers. These results are in good agreement with data obtained from electrophysiological recordings, which reveal reduction in neural plasticity following cannabinoid treatment, and increased plasticity following antagonist exposure. The mixed receptor properties of the pharmacological tool, however, make it difficult to define the exact role of any CB1 receptor population in memory processes with any certainty. This makes it all the more important that behavioural studies use selective administration of drugs to specific brain areas, rather than global administration to whole animals. The emerging role of the endogenous cannabinoid system in the hippocampus may be to facilitate the induction of long-term potentiation/the encoding of information. Administration of exogenous selective CB1 agonists may therefore disrupt hippocampus-dependent learning and memory by ’increasing the noise’, rather than ’decreasing the signal’ at potentiated inputs.
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References
Adams AJ, Brown B, Haegerstrom-Portnoy G, Flom MC (1976) Evidence for acute effects of alcohol and marijuana on color discrimination. Percept Psychophys 20:119–124
Aiger TG (1988) Delta-9-tetrahydrocannabinol impairs visual recognition memory but not discrimination learning in rhesus monkeys. Psychopharmacology (Berl) 95:507–511
Al-Hayani A, Davies SN (2000) Cannabinoid receptor mediated inhibition of excitatory synaptic transmission in the rat hippocampal slice is developmentally regulated. Br J Pharmacol 131:663–665
Ameri A, Simmet T (2000) Effects of 2-arachidonylglycerol, an endogenous cannabinoid, on neuronal activity in rat hippocampal slices. Naunyn Schmiedebergs Arch Pharmacol 361:265–272
Arizzi MN, Cervone KM, Aberman JE, Betz A, Liu Q, Lin S, Markiyannis A, Salamone JD (2004) Behavioral effects of inhibition of cannabinoid metabolism: The amidase inhibitor AM374 enhances the suppression of lever pressing produced by exogenously administered anandamide. Life Sci 74:1001–1011
Auclair N, Oyani S, Soubrie P, Crepel F (2000) Cannabinoids modulate synaptic strength and plasticity at glutamatergic synapses of rat prefrontal cortex pyramidal neurons. J Neurphysiol 83:3287–3293
Barabara J-G, Auclair N, Roisin M-P, Otani S, Valjent E, Caboche J, Soubrie P, Crepel F (2003) Direct and indirect interactions between cannabinoid CB1 receptor and group II metabotropic glutamate receptor signalling in layer V pyramidal neurons from the rat prefrontal cortex. Eur J Neurosci 17:981–990
Barros DM, Carlis V, Maidana M, Silva AS, Baisch ALM, Ramirez MR, Izquierdo I (2004) Interactions between anandamide-induced anterograde amnesia and post-trainingmemory modulatory systems. Brain Res 1016:66–71
Bech P, Rafaelsen L, Rafaelsen OJ (1973) Cannabis and alcohol: Effects on estimation of time and distance. Psychopharmacologia 32:373–381
Biegon A, Kerman I (1995) Quantitative autoradiography of cannabinoid receptors in the human brain post-mortem. In: Biegon A, Volkow ND (eds) Sites of drug action in the human brain. CRC Press, Boca Raton, pp 65–74
Block RI, O’Leary DS, Ehrhardt JC, Augustinack JC, Ghonheim MM, Arndt S, Hall JA (2000) Effects of frequentmarijuana use on brain tissue volume and composition. NeuroReport 11:491–496
Block RI, O’Leary DS, Hichwa RD, Augustinack JC, Boles Ponto LL, Ghonheim MM, et al (2002) Effects of frequent marijuana use on memory-related regional cerebral blood flow. Pharmacol Biochem Behav 72:237–250
Bohme GA, Laville M, Ledent C, Parmentier M, Imperato A (2000) Enhanced long-term potentiation in mice lacking cannabinoid CB1 receptors. Neuroscience 95:5–7
Borg J, Gershon S, Alpert M (1975) Dose effects of smoked marijuana on human cognitive and motor functions. Psychopharmacologia 42:211–218
Bowman M, Pihl RO (1973) Cannabis: psychological effects of chronic heavy use: a controlled study of intellectual functioning in chronic users of high potency cannabis. Psychopharmacologia 29:159–190
Braden W, Stillman RC, Wyatt RJ (1974) Effects of marijuana on contingent negative variation and reaction time. Arch Gen Psychiatry 31:537–541
Branch MN, Dearing ME, Lee DM (1980) Acute and chronic effects of Δ9-tetrahydrocannabinol on complex behavior in squirrelmonkeys. Psychopharmacology (Berl) 71:247–256
Breivogel CS, Griffin G, Di Marzo V, Martin BR (2001) Evidence for a new G protein-coupled cannabinoid receptor in mouse brain. Mol Pharmacol 60:155–163
Brodkin J, Moerschbacher JM (1997) SR141716A antagonizes the disruptive effects of cannabinoid ligands on learning in rats. J Pharmacol Exp Ther 282:1526–1532
Carlson G, Wang Y, Alger BE (2002) Endocannabinoids facilitate the induction of LTP in the hippocampus. Nat Neurosci 5:723–724
Castellano C, Cabib S, Palmisano A, et al (1997) The effects of anandamide on memory consolidation in mice involve both D1 and D2 dopamine receptors. Behav Pharmacol 8:707–712
Castellano C, Ventura R, Caibb S, et al (1999) Strain-dependent effects of anandamide on memory consolidation in mice are antagonized by naltrexone. Behav Pharmacol 10:453–457
Chait LD, Pierri J (1992) Effects of smoked marijuana on human performance: a critical review. In: Murphy L, Bartke A (eds) Marijuana/cannabinoids: Neurobiology and neurophysiology. CRC Press, Boca Raton, pp 387–423
Chevaleyre V, Castillo PE (2003) Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron 38:461–472
Ciccocioppo R, Antonelli L, Biondini M, et al (2002) Memory impairment following combined exposure to Δ9-tetrahydrocannabinol and ethanol in rats. Eur J Pharmacol 449:245–252
Clark LD, Nakashima EN (1968) Experimental studies of marijuana. Am J Psychiatry 125:379–384
Cohen J (1990) Statistical power analysis for the behavioural sciences. Lawrence Earlbaum Publishers, Hillsdale, NJ
Collins DR, Pertwee RG, Davies SN (1995) Prevention by the cannabinoid antagonist, SR141716A, of cannabinoid-mediated blockade of long-term potentiation in the rat hippocampal slice. Br J Pharmacol 115:869–870
Collins DR, Pertwee RG, Davies SN (1994) The actions of synthetic cannabinoids on the induction of long-term potentiation in the rat hippocampal slice. Eur J Pharmacol 259:R7–R8
Crawley JN (2000) What is wrong with my mouse? Wiley-Liss, New York
Da Silva GE, Takahashi RN (2002) SR141716A prevents Δ9-tetrahydrocannabinol-induced spatial learning deficit in a Morris-type water maze in mice. Prog Neuropsychopharmacol Biol Psychiatry 26:321–325
Deadwyler SA, Hampson RE (1999) Anatomic model of hippocampal encoding of spatial information. Hippocampus 9:397–412
Deadwyler SA, Heyser CJ, Hampson RE (1995) Complete adaptation to the memory disruptive effects of delta-9-THC following 35 days of exposure. Neurosci Res Commun 17:9–18
Deadwyler SA, Bunn T, Hampson RE (1996) Hippocampal ensemble activity during spatial delayed-nonmatch-to-sample performance in rats. J Neurosci 16:354–372
DeSanty KP, Dar MS (2001a) Cannabinoid-induced motor incoordination through the cerebellar CB1 receptor in mice. Pharmacol Biochem Behav 69:251–259
DeSanty KP, Dar MS (2001b) Involvement of the cerebellar adenosine A1 receptor in cannabinoid-induced motor incoordination in the acute and tolerant state in mice. Brain Res 905:178–187
Di Marzo V, Goparaju SK, Wang L, et al (2001) Leptin-regulated endocannabinoids are involved in maintaining food intake. Nature 410:822–825
Diana G, Pieri M, Valentini G (2002) Effects of WIN55,212-2 on hippocampal CA1 long-term potentiation in experiments controlled for basal glutamatergic synaptic transmission. Eur J Pharmacol 453:251–254
Diana G, Malloni, M, Pieri M (2003) Effects of the synthetic cannabinoid nabilone on spatial learning and hippocampal transmission. Pharmacol Biochem Behav 75:585–591
Dornbush RL (1974) Marijuana and memory: effects of smoking on storage. Trans N Y Acad Sci 36:94–100
Dornbush RL, Fink M, Freedman AM (1971) Marijuana, memory and perception. Am J Psychiatry 128:194–197
Earleywine M, Newcomb M (1997) Concurrent versus simultaneous polydrug use: prevalence, correlates, discriminant validity, and prospective effects on health outcomes. Exp Clin Psychopharmacol 5:353–364
Elwan O, Hassan AAH, Naseer MA, Elwan F, et al (1997) Brain aging in a sample of normal Egyptians: cognition, education, addiction and smoking. J Neurol Sci 148:79–86
Ennaceur A, Delacour J (1988) A new one-trial test for neurobiological studies of memory in rats. I. Behavioral data. Behav Brain Res 31:47–59
Entin EE, Glodzung PJ (1973) Residual effects of marijuana use on learning and memory. Psychol Rec 23:169–178
Evans EB, Wenger GR (1992) Effects of drugs of abuse on acquisition of behavioral chains in squirrel monkeys. Psychopharmacology (Berl) 107:55–60
Evans MA, Martz R, Rodda BE, Lemberger L, Forney RB (1976) Effects of marihuanadextroamphetamine combination. Clin Pharmacol Ther 20:350–361
Ferrari F, Ottani A, Vivoli R, et al (1999) Learning impairment produced in rats by the cannabinoid agonist HU210 in a water-maze task. Pharmacol Biochem Behav 64:555–561
Fletcher JM, Page JB, Francis DJ, et al (1996) Cognitive correlates of long-termcannabis use in Costa Rican men. Arch Gen Psychiatry 53:1051–1057
Gaoni Y, Mechoulam R (1964) Isolation, structure and partial synthesis of an active constituent of hashish. J Am Chem Soc 86:1646–1647
Gerdeman GL, Ronesi J, Lovinger DM (2002) Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nature Neurosci 5:446–451
Gianutsos R, Litwack AR (1976) Chronic marijuana smokers show reduced coding into long-term storage. Bull Psychon Soc 7:277–279
Gluck JP, Ferraro DP, Marriott RG (1973) Retardation of discrimination reversal by delta-9-tetrahydrocannabinol in monkeys. Pharmacol Biochem Behav 1:605–608
Hajos N, Freund TF (2002) Pharmacological separation of cannabinoid sensitive receptors on hippocampal excitatory and inhibitory fibres. Neuropharmacology 43:503–510
Hajos N, Ledent C, Freund TF (2001) Novel cannabinoid-sensitive receptor mediates inhibition of glutamatergic synaptic transmission in the hippocampus. Neuroscience 106:1–4
Hampson RE, Deadwyler S (2000) Cannabinoids reveal the necessity of hippocampal neural encoding for short-term memory in rats. J Neurosci 20:8932–8942
Hampson RE, Deadwyler SA (1996) Ensemble codes involving hippocampal neurons are at risk during delayed performance tests. Proc Natl Acad Sci USA 93:13487–13493
Hampson RE, Deadwyler SA (1998) Role of cannabinoid receptors in memory storage. Neurobiol Dis 5:474–482
Hampson RE, Deadwyler SA (1999) Cannabinoids, hippocampal function and memory. Life Sci 65:715–723
Hampson RE, Heyser CJ, Deawyler SA (1993) Hippocampal cell firing correlates of delayed match-to-sample performance in the rat. Behav Neurosci 107:715–739
Hampson RE, Jarrard LE, Deadwyler SA (1999a) Effects of ibotenate hippocampal destruction on delayed matching and nonmatching to sample behavior in rats. J Neurosci 19:1492–1507
Hampson RE, Simeral JD, Deadwyler SA (1999b) Distribution of spatial and nonspatial information in dorsal hippocampus. Nature 402:610–614
Han CJ, Robinson JK (2001) Cannabinoid modulation of time estimation in the rat. Behav Neurosci 115:243–246
Han CJ, Pierre-Louis J, Scheff A, et al (2000) A performance-dependent adjustment of the retention interval in the delayed non-matching-to-position paradigm differentiates effects of amnestic drugs in rats. Eur J Pharmacol 403:87–93
Hernandez-Tristan R, Arevalo C, Canals S, et al (2000) The effects of acute treatment with Delta(9)-THC on exploratory behaviour and memory in the rat. J Physiol Biochem 56:17–24
Heyser CJ, Hampson RE, Deadwyler SA (1993) Effects of delta-9-tetrahydrocannabinol on delayed match to sample performance in rats. Alterations in short-term memory associated with changes in task specific firing of hippocampal cells. J Pharmacol Exp Ther 264:294–307
Hoffman AF, Oz M, Caulder T, Lupicia 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
Isaacson RL, Douglas RJ, Moore RY (1961) The effect of radical hippocampal ablation on acquisition of avoidance response. J Comp Physiol Psychol 54:625–628
Izquierdo I, Nasello AG (1973) Effects of cannabidiol and diphenyl hydantoin on the hippocampus and learning. Psychopharmacologia 31:167–175
Järbe TUC, Hiltunen AJ (1987) Cannabimimetic activity of cannabinol in rats and pigeons. Neuropharmacology 26:219–228
Järbe TUC, Andrzejewski ME, DiPatrizio NV (2002) Interaction between the CB1 receptor agonist Δ9-THC and the CB1 receptor antagonist SR-141716 in rats. Open field revisited. Pharmacol Biochem Behav 73:911–919
Jarrard LE (1993) On the role of the hippocampus in learning and memory in the rat. Behav Neural Biol 60:9–26
Jentsch JD, Andrusiak E, Tran A, et al (1996) HA966 prevents increases in prefrontal dopamine turnover and impairments in spatial working memory induced by psychomimetic drugs. FASEB J 20:A716
Jentsch JD, Andrusiak E, Tran A, et al (1997) Δ9-Tetrahydrocannabinol increases prefrontal cortical catecholaminergic utilisation and impairs spatial working memory in the rat: blockade of dopaminergic effects by HA966. Neuropsychopharmacology 16:426–432
Johnson JP, Muhleman D, MacMurray J, et al (1997) Association between the cannabinoid receptor gene (CNR1) and the P300 event-related potential. Mol Psychiatry 2:169–171
Katona I, Rancz EA, Acsady L, Ledent C, Mackie K, Hajos N, Freund TF (2001) Distribution of CB1 cannabinoid receptors in the amygdala and their role in the control of GABAergic transmission. J Neurosci 21:9506–9518
Kim J, Isokawa M, Ledent C, Alger BE (2002) Activation of muscarinic acetylcholine receptors enhances the release of endogenous cannabinoids in the hippocampus. J Neurosci 22:10182–10191
Koch M (1999) The neurobiology of startle. Prog Neurobiol 59:107–128
Kosiorek P, Hryniewicz A, Bialuk I, Zawadzka A, Winnicka A (2003) Cannabinoids alter recognition memory in rats. Pol J Pharmacol 55:903–910
Kreitzer AC, Regehr WG (2001) Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29:717–727
Levenes C, Daniel H, Soubrie P, Crepel F (1998) Cannabinoids decrease excitatory synaptic transmission and impair long-term depression in rat cerebellar Purkinje cells. J Physiol 510:867–879
Lichtman AH (2000) SR141716A enhances spatial memory assessed in a radial-arm maze task in rats. Eur J Pharmacol 404:175–179
Lichtman AH, Martin BR (1996) Δ9-Tetrahydrocannabinol impairs spatial memory through cannabinoid receptor mechanism. Psychopharmacology (Berl) 126:125–131
Lichtman AH, Martin BR (1997) The selective cannabinoid antagonist SR 141716A blocks cannabinoid-induced antinociception in rats. Pharmacol Biochem Behav 57:7–12
Lichtman AH, Dimen KR, Martin BR (1995) Systemic or intrahippocampal cannabinoid administration impairs spatial memory in rats. Psychopharmacology (Berl) 119:282–290
Lichtman AH, Varvel SA, Martin BR (2002) Endocannabinoids in cognition and dependence. Prostaglandins Leukot Essent Fatty Acids 66:269–285
Lyketsos CG, Garret E, Liang KY, Anthony JC (1999) Cannabis use and cognitive decline in persons under 65 years of age. Am J Epidemiol 149:794–800
Maccarrone M, Valverde O, Barbaccia ML, et al (2002) Age-related changes of anandamide metabolism in CB1 cannabinoid receptor knockout mice: correlation with behaviour. Eur J Neurosci 15:1178–1186
Maejima T, Hashimoto K, Yoshida T, Aiba A, Kano M (2001) Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabinoid receptors. Neuron 31:463–475
Mallet PE, Beninger RJ (1996) The endogenous cannabinoid receptor agonist impairs memory in rats. Behav Pharmacol 7:276–284
Mallet PE, Beninger RJ (1998) The cannabinoid CB1 receptor antagonist SR141716A attenuates the memory impairment produced by Δ9-tetrahydrocannabinol or anandamide. Psychopharmacology (Berl) 140:11–19
Mansbach RS, Rovetti CC, Winston EN, et al (1996) Effects of cannabinoid receptor antagonist SR141716A on the behavior of pigeons and rats. Psychopharmacology (Berl) 124:315–322
Marsciano G, Wotjack CT, Azas SC, Bisogno T, Rammes G, Cascio MG, Hermann H, Tang J, Hofmann C, Zieglgänsberger W, Di Marzo V, Lutz B (2002) The endogenous cannabinoid system controls extinction of aversive memories. Nature 418:530–534
Martin M, Ledent C, Parmentier M, Maldonado R, Valverde O (2002) Involvement of CB1 cannabinoid receptors in emotional behaviour. Psychopharmacology (Berl) 159:379–387
Mathew RJ, Wilson WH (1991) Substance abuse and cerebral blood flow. Am J Psychiatry 148:292
Mechoulam R, Fride E (2001) A hunger for cannabinoids. Nature 410:763–765
Menhiratta SS, Wig NN, Verma SK (1978) Some psychological correlates of long-term heavy cannabis users. Br J Psychiatry 132:482–486
Mereu G, Fà M, Ferraro L, Cagiano R, Antonelli T, Tattoli M, Ghiglieri V, Tanganelli S, Gessa GL, Cuomo V (2003) Prenatal exposure to a cannabinoid agonist produces memory deficits linked to dysfunction in hippocampal long-term potentiation and glutamate release. Proc Natl Acad Sci USA 100:4915–4920
Miller L, Cornett T (1978) Marijuana: dose-response effects on pulse rate, subjective estimates of intoxication, free recall and recognition memory. Pharmacol Biochem Behav 9:573–579
Mishima K, Egashira N, Hirosawa N, et al (2001) Characteristics of learning and memory impairment induced by Δ9-tetrahydrocannabinol in rats. Jpn J Pharmacol 87:297–308
Misner DL, Sullivan JM (1999) Mechanism of cannabinoid effects on long-term potentiation and depression in hippocampal CA1 neurons. J Neurosci 19:6795–6805
Miyamoto A, Yamamoto T, Watanabe S (1995) Effect of repeated administration of Δ9-tetrahydrocannabinol on delayed matching-to-sample performance in rats. Neurosci Lett 201:139–142
Molina-Holgado F, Gonzalez MI, Leret ML (1995) Effect of Δ9-tetrahydocannabinol on short-term memory in the rat. Physiol Behav 57:177–179
Morris RGM (1984) Developments of a water-maze procedure for studying spatial learning in that rat. J Neurosci Methods 11:47–60
Nakamura EM, da Silva EA, Concilio GV, et al (1991) Reversible effects of acute and longterm administration of Δ-9-tetrahydrocannabinol (THC) on memory in the rat. Drug Alcohol Depend 28:167–175
Nakamura-Palacios EM, Winsauer PJ, Moerschbacher JM (2000) Effects of the cannabinoid ligand SR141716A alone or in combination with Δ9-tetrahydrocannabinol or scopolamine on learning in squirrel monkeys. Behav Pharmacol 11:377–389
Nava F, Carta G, Battesi AM, et al (2000) D2 dopamine receptors enable Δ9-tetrahydrocannabinol induced memory impairment and reduction of hippocampal extracellular acetylcholine concentration. Br J Pharmacol 130:1201–1210
Nava F, Carta G, Colombo G, et al (2001) Effects of chronic Δ9-tetrahydrocannabinol treatment on hippocampal extracellular acetylcholine concentration and alternation performance in the T-maze. Neuropharmacology 41:392–399
Navarro M, Fernandez Ruiz JJ, de Miguel R, et al (1993) Motor disturbances induced by an acute dose of Δ9-tetrahydrocannabinol: possible involvement of nigrostriatal dopaminergic alterations. Pharmacol Biochem Behav 45:291–298
Nowicky AV, Teyler TJ, Vardaris RM (1987) The modulation of long-term potentiation by delta-9-tetrahydrocannabinol in the rat hippocampus, in vitro. Brain Res Bull 19:663–672
O’Leary DS, Block RI, Koeppel JA, et al (2002) Effects of smoking marijuana on brain perfusion and cognition. Neuropsychopharmacology 26:802–816
Ohno-Shosaku T, Maejima T, Kano M (2001) Endogenous cannabinoids mediate retrograde signals fromdepolarised postsynaptic neurons to presynaptic terminals. Neuron 29:729–738
Ohno-Shosaku T, Tsubokawa H, Mizushima I, Yoneda N, Zimmer A, Kano M (2002) Presynaptic cannabinoid sensitivity is a major determinant of depolarization-induced retrograde suppression at hippocampal synapses. J Neurosci 22:3864–3872
Onaivi ES, Green MR, Martin BR (1990) Pharmacological characterisation of cannabinoids in the elevated plus-maze. J Pharmacol Exp Ther 253:1002–1009
Paton GS, Pertwee RG, Davies SN (1998) Correlation between cannabinoid mediated effects on paired pulse depression and induction of long term potentiation in the rat hippocampal slice. Neuropharmacology 37:1123–1130
Patrick G, Straumanis JJ, Struve FA, Fitz-Gerald MJ, Leavitt J, Manno JE (1999) Reduced P50 auditory gating response in psychiatrically normal chronic marihuana users: a pilot study. Biol Psychiatry 45:1307–1312
Pearl J, Domino E, Rennick P (1973) Short-term effects of marijuana smoking on cognitive behavior in experienced male users. Psychopharmacologia 31:13–24
Pertwee RG (1997) Pharmacology of cannabinoid CB1 and CB2 receptors. Pharmacol Ther 74:129–180
Pitler TA, Alger BE (1992) Postsynaptic spike firing reduces synaptic GABA(A) responses in hippocampal pyramidal cells. J Neurosci 12:4122–4132
Pope HG, Yurgelun-Todd D (1996) The residual cognitive effects of heavy marijuana use in college students. J Am Med Assoc 275:521–527
Porter AC, Felder CC (2001) The endocannabinoid nervous system: Unique opportunities for therapeutic intervention. Pharmacol Ther 90:45–60
Presburger G, Robinson JK (1999) Spatial signal detection in rats is differentially disrupted by Δ-9-tetrahydrocannabinol, scopolamine and MK-801. Behav Brain Res 99:27–34
Reibaud M, Obinu MC, Ledent C, et al (1999) Enhancement of memory in cannabinoid CB1 receptor knock-out mice. Eur J Pharmacol 379:R1–R2
Robbe D, Alonso G, Duchamp F, Bockaert J, Manzoni JM (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, Kopf M, Remaury A, Bockaert J, Manzoni O (2002) Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc Natl Acad Sci USA 99:8384–8388
Robbe D, Alonso G, Manzoni O (2003) Exogenous and endogenous cannabinoids control synaptic transmission in mice nucleus accumbens. Ann NY Acad Sci 1003:212–225
Robinson L, Hinder L, Pertwee RG, Riedel G (2003) Effects of Δ9-THC and WIN-55,212-2 on place preference in the water maze in rats. Psychopharmacology (Berl) 166:40–50
Rochford J, Grant I, LaVigne G (1977) Medical students and drugs: Further neuropsychological and use pattern considerations. Int J Addict 12:1057–1065
Rodriguez de Fonseca F, Del Arco I, Martin-Calderon JL, et al (1998) Role of the endogenous cannabinoid system in the regulation of motor activity. Neurobiol Dis 5:483–501
Satz P, Fletcher JM, Sutker LS (1976) Neuropsychologic, intellectual and personality correlates in chronic marihuana use in native Costa Ricans. Ann NY Acad Sci 282:266–306
Schneider M, Koch M (2002) The cannabinoid agonist WIN 55,212-2 reduces sensorimotor gating and recognition memory in rats. Behav Pharmacol 13:29–37
Schulze GE, McMillan DE, Bailey JR, et al (1988) Acute effects of delta-9-tetrahydrocannabinol in rhesus monkeys as measured by performance in a battery of complex operant tests. J Pharmacol Exp Ther 245:178–186
Schwartz RH, Gruenewald PJ, Klitzner M, et al (1989) Short-term memory impairments in cannabis-dependent adolescents. Am J Dis Child 143:1214–1219
Schweitzer P, Siggins GR, Madamba SG (1999) Cannabinoid modulation of neuronal activity in adult rat hippocampus. Adv Exp Med Biol 469:547–552
Sjöström PJ, Turrigano GG, Nelson SB (2003) Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron 39:641–654
Solowij N (1998) Cannabis and cognitive functioning. Cambridge University Press, Cambridge
Soueif MI (1976) Some determinant of psychological deficits associated with chronic cannabis consumption. Bull Narc 28:25–42
Stadnicki SW, Schaeppi U, Rosenkrantz H, et al (1974) Crude marihuana extract: EEG and behavioral effects of chronic oral administration in rhesus monkeys. Psychopharmacologia 37:225–233
Stella N, Schweitzer P, Piomelli D (1997) A second endogenous cannabinoid that modulates long-term potentiation. Nature 388:773–778
Stiglick A, Kalant H (1982) Learning impairment in the radial-arm maze following prolonged cannabis treatment in rats. Psychopharmacology (Berl) 77:117–123
Stiglick A, Llewellyn ME, Kalant H (1984) Residual effects of prolonged cannabis treatment on shuttle-box avoidance in the rat. Psychopharmacology (Berl) 84:476–479
Strohmetz DB, Alterman AI, Walter D (1990) Subject selection bias in alcoholics volunteering for a treatment study. Alcohol Clin Exp Res 14:736–738
Struve FA, Straumanis JJ, Patrick G (1994) Persistent topographic quantitative EEG sequelae of chronic marijuana use: A replication study and initial discriminant function analysis. Clin Electroencephalogr 25:63–75
Szallasi A, Di Marzo V (2000) New perspectives on enigmatic vanilloid receptors. Trends Neurosci 23:491–497
Tart CT (1971) On being stoned. Science and Behavior Books, Palo Alto
Teng AH, Craft RM (2004) CB1 receptor mediation of cannabinoid behavioural effects in male and female rats. Psychopharmacology (Berl) 172:25–30
Terranova J-P, Michaud J-C, Le Fur G, Soubrie P (1995) Inhibition of long-term potentiation in rat hippocampal slices by anandamide and WIN55,212-2: reversal by SR141716A, a selective antagonist of CB1 cannabinoid receptors. Naunyn Schmiedebergs Arch Pharmacol 352:576–579
Terranova J-P, Storme J-J, Lafon N, et al (1996) Improvement of memory in rodents by the selective CB1 cannabinoid receptor antagonist, SR141716. Psychopharmacology (Berl) 126:165–172
Varma N, Carlson GC, Ledent C, Alger BE (2001) Metabotropic glutamate receptors drive the endocannabinoid system in hippocampus. J Neurosci 21:RC188
Varvel SA, Lichtman AH (2002) Evaluation of CB1 receptor knockout mice in the Morris water maze. J Pharmacol Exp Ther 301:915–924
Varvel SA, Hamm RJ, Martin BR, et al (2001) Differential effects of Δ9THC on spatial reference and working memory in mice. Psychopharmacology (Berl) 157:142–150
Westlake GA, Howlett AC, Bonner TI, Matsuda LA, Herkenham M (1994) Cannabinoid receptor binding and messenger RNA expression in human brain: an in vitro receptor autoradiography and in situ hybridization histochemistry study of normal and Alzheimer’s brains. Neuroscience 63:637–652
Wig NN, Verma SK (1977) Patterns of long-term heavy cannabis use in north India and its effects on cognitive functions: A preliminary report. Drug Alcohol Depend 2:211–219
Wilson RI, Nicoll RA (2001) Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410:588–592
Wilson RI, Nicoll RA (2002) Endocannabinoid signalling in the brain. Science 296:678–682
Wilson WH, Mathew RJ (2002) Effects of marijuana on brain: Function and structure. In: Onaivi ES (ed) Biology of marijuana: from gene to behavior. Taylor and Francis, London, pp 234–281
Winsauer PJ, Lambert P, Moerschbacher JM (1999) Cannabinoid ligands and their effects on learning and performance in rhesus monkeys. Behav Pharmacol 10:497–511
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Riedel, G., Davies, S.N. (2005). Cannabinoid Function in Learning, Memory and Plasticity. In: Pertwee, R.G. (eds) Cannabinoids. Handbook of Experimental Pharmacology, vol 168. Springer, Berlin, Heidelberg. https://doi.org/10.1007/3-540-26573-2_15
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