The acute effects of cannabinoids on memory in humans: a review (original) (raw)

• Abel EL (1971) Marihuana and memory: acquisition or retrieval? Science 173:1038–1040
  PubMed CAS Google Scholar
• Abel T, Lattal KM (2001) Molecular mechanisms of memory acquisition, consolidation and retrieval. Curr Opin Neurobiol 11:180–187
  PubMed CAS Google Scholar
• Acquas E, Pisanu A, Marrocu P, Di Chiara G (2000) Cannabinoid CB(1) receptor agonists increase rat cortical and hippocampal acetylcholine release in vivo. Eur J Pharmacol 401:179–185
  PubMed CAS Google Scholar
• Acquas E, Pisanu A, Marrocu P, Goldberg SR, Di Chiara G (2001) Delta9-tetrahydrocannabinol enhances cortical and hippocampal acetylcholine release in vivo: a microdialysis study. Eur J Pharmacol 419:155–161
  PubMed CAS Google Scholar
• Adams IB, Martin BR (1996) Cannabis: pharmacology and toxicology in animals and humans. Addiction 91:1585–1614
  PubMed CAS Google Scholar
• Agurell S, Halldin M, Lindgren JE, Ohlsson A, Widman M, Gillespie H, Hollister L (1986) Pharmacokinetics and metabolism of delta 9-tetrahydrocannabinol and other cannabinoids with emphasis on man. Pharmacol Rev 38:21–43
  PubMed CAS Google Scholar
• Aigner TG (1988) Delta-9-tetrahydrocannabinol impairs visual recognition memory but not discrimination learning in rhesus monkeys. Psychopharmacology (Berl) 95:507–511
  CAS Google Scholar
• Atkinson R, Shiffrin RM (1968) Human memory: a proposed system and its control processes. New York Academic Press, New York
  Google Scholar
• Baddeley A (1999) Essentials of human memory. Psychology Press
• Baddeley A, Chincotta D, Adlam A (2001) Working memory and the control of action: evidence from task switching. J Exp Psychol Gen 130:641–657
  PubMed CAS Google Scholar
• Baker D, Pryce G, Davies WL, Hiley CR (2006) In silico patent searching reveals a new cannabinoid receptor. Trends Pharmacol Sci 27:1–4
  PubMed CAS Google Scholar
• Belmore SM, Miller LL (1980) Levels of processing and acute effects of marijuana on memory. Pharmacol Biochem Behav 13:199–203
  PubMed CAS Google Scholar
• Block RI, Farinpour R, Braverman K (1992) Acute effects of marijuana on cognition: relationships to chronic effects and smoking techniques. Pharmacol Biochem Behav 43:907–917
  PubMed CAS Google Scholar
• 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
  PubMed CAS Google Scholar
• Brodkin J, Moerschbaecher JM (1997) SR141716A antagonizes the disruptive effects of cannabinoid ligands on learning in rats. J Pharmacol Exp Ther 282:1526–1532
  PubMed CAS Google Scholar
• Budney AJ, Moore BA, Vandrey RG, Hughes JR (2003) The time course and significance of cannabis withdrawal. J Abnorm Psychology 112:393–402
  Google Scholar
• Budney AJ, Hughes JR, Moore BA, Vandrey R (2004) Review of the validity and significance of cannabis withdrawal syndrome. Am J Psychiatry 161:1967–1977
  PubMed Google Scholar
• Buschke H, Fuld PA (1974) Evaluating storage, retention, and retrieval in disordered memory and learning. Neurology 24:1019–1025
  PubMed CAS Google Scholar
• Carlini EA, Hamaoui A, Bieniek D, Korte F (1970a) Effects of (−) delta-9-trans-tetrahydrocannabinol and a synthetic derivative on maze performance of rats. Pharmacology 4:359–368
  PubMed CAS Google Scholar
• Carlini EA, Santos M, Claussen U, Bieniek D, Korte F (1970b) Structure activity relationship of four tetrahydrocannabinols and the pharmacological activity of five semi-purified extracts of Cannabis sativa. Psychopharmacologia 18:82–93
  PubMed CAS Google Scholar
• Castellano C, Rossi-Arnaud C, Cestari V, Costanzi M (2003) Cannabinoids and memory: animal studies. Curr Drug Targets CNS Neurol Disord 2:389–402
  PubMed CAS Google Scholar
• Chait LD, Perry JL (1994) Acute and residual effects of alcohol and marijuana, alone and in combination, on mood and performance. Psychopharmacology (Berl) 115:340–349
  CAS Google Scholar
• Chait LD, Zacny JP (1992) Reinforcing and subjective effects of oral delta 9-THC and smoked marijuana in humans. Psychopharmacology 107:255–262
  Google Scholar
• Chen J, Paredes W, Lowinson JH, Gardner EL (1990) Delta 9-tetrahydrocannabinol enhances presynaptic dopamine efflux in medial prefrontal cortex. Eur J Pharmacol 190:259–262
  PubMed CAS Google Scholar
• Collins DR, Pertwee RG, Davies SN (1994) The action of synthetic cannabinoids on the induction of long-term potentiation in the rat hippocampal slice. Eur J Pharmacol 259:R7–R8
  PubMed CAS Google Scholar
• Compton DR, Johnson MR, Melvin LS, Martin BR (1992) Pharmacological profile of a series of bicyclic cannabinoid analogs: classification as cannabimimetic agents. J Pharmacol Exp Ther 260:201–209
  PubMed CAS Google Scholar
• Curran HV, Brignell C, Fletcher S, Middleton P, Henry J (2002) Cognitive and subjective dose–response effects of acute oral Delta 9-tetrahydrocannabinol (THC) in infrequent cannabis users. Psychopharmacology (Berl) 164:61–70
  CAS Google Scholar
• Da Silva GE, Takahashi RN (2002) SR 141716A prevents delta 9-tetrahydrocannabinol-induced spatial learning deficit in a Morris-type water maze in mice. Prog neuropsychopharmacol Biol Psychiatry 26:321–325
  Google Scholar
• Darley CF, Tinklenberg JR, Hollister TE, Atkinson RC (1973) Marihuana and retrieval from short-term memory. Psychopharmacologia 29:231–238
  PubMed CAS Google Scholar
• Darley CF, Tinklenberg JR, Roth WT, Atkinson RC (1974) The nature of storage deficits and state-dependent retrieval under marihuana. Psychopharmacologia 37:139–149
  PubMed CAS Google Scholar
• Davies SN, Pertwee RG, Riedel G (2002) Functions of cannabinoid receptors in the hippocampus. Neuropharmacology 42:993–1007
  PubMed CAS Google Scholar
• de Oliveira Alvares L, de Oliveira LF, Camboim C, Diehl F, Genro BP, Lanziotti VB, Quillfeldt JA (2005) Amnestic effect of intrahippocampal AM251, a CB1-selective blocker, in the inhibitory avoidance, but not in the open field habituation task, in rats. Neurobiol Learn Mem 83:119–124
  PubMed Google Scholar
• Demuth DG, Molleman A (2005) Cannabinoid signalling. Life Sci 78:549–563
  PubMed Google Scholar
• Dhawan J, Deng H, Gatley SJ, Makriyannis A, Akinfeleye T, Bruneus M, Dimaio AA, Gifford AN (2006) Evaluation of the in vivo receptor occupancy for the behavioral effects of cannabinoids using a radiolabeled cannabinoid receptor agonist, R-[(125/131)I]AM2233. Synapse 60:93–101
  PubMed CAS Google Scholar
• Diana M, Melis M, Gessa GL (1998) Increase in meso-prefrontal dopaminergic activity after stimulation of CB1 receptors by cannabinoids. Eur J Neurosci 10:2825–2830
  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
  PubMed CAS Google Scholar
• D’Souza DC, Abi-Saab WM, Madonick S, Forselius-Bielen K, Doersch A, Braley G, Gueorguieva R, Cooper TB, Krystal JH (2005) Delta-9-tetrahydrocannabinol effects in schizophrenia:implications for cognition, psychosis, and addiction. Biol Psychiatry 57:594–608
  PubMed CAS Google Scholar
• Dudai Y (2004) The neurobiology of consolidations, or, how stable is the engram? Annu Rev Psychol 55:51–86
  PubMed Google Scholar
• Dudai Y, Eisenberg M (2004) Rites of passage of the engram: reconsolidation and the lingering consolidation hypothesis. Neuron 44:93–100
  PubMed CAS Google Scholar
• Fant RV, Heishman SJ, Bunker EB, Pickworth WB (1998) Acute and residual effects of marijuana in humans. Pharmacol Biochem Behav 60:777–784
  PubMed CAS Google Scholar
• Ferraro DP (1980) Acute effects of marijuana on human memory and cognition. NIDA Res Monogr 31:98–119
  PubMed CAS Google Scholar
• Ferraro DP, Grilly DM (1974) Effects of chronic exposure to delta9-tetrahydrocannabinol on delayed matching-to-sample in chimpanzees. Psychopharmacologia 37:127–138
  PubMed CAS Google Scholar
• Fletcher PC, Henson RN (2001) Frontal lobes and human memory: insights from functional neuroimaging. Brain 124:849–881
  PubMed CAS Google Scholar
• Freedland CS, Whitlow CT, Miller MD, Porrino LJ (2002) Dose-dependent effects of Delta9-tetrahydrocannabinol on rates of local cerebral glucose utilization in rat. Synapse 45:134–142
  PubMed CAS Google Scholar
• Gerard CM, Mollereau C, Vassart G, Parmentier M (1991) Molecular cloning of a human cannabinoid receptor which is also expressed in testis. Biochem J 279:129–134
  PubMed 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
  PubMed CAS Google Scholar
• Gessa GL, Casu MA, Carta G, Mascia MS (1998) Cannabinoids decrease acetylcholine release in the medial-prefrontal cortex and hippocampus, reversal by SR 141716A. Eur J Pharmacol 355:119–124
  PubMed CAS Google Scholar
• Greenwald MK, Stitzer ML (2000) Antinociceptive, subjective and behavioral effects of smoked marijuana in humans. Drug Alcohol Depend 59:261–275
  PubMed CAS Google Scholar
• Grotenhermen F (2003) Pharmacokinetics and pharmacodynamics of cannabinoids. Clin Pharmacokinet 42:327–360
  PubMed CAS Google Scholar
• Hajos N, Katona I, Naiem SS, MacKie K, Ledent C, Mody I, Freund TF (2000) Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations. Eur J Neurosci 12:3239–3249
  PubMed CAS Google Scholar
• Hajos N, Ledent C, Freund TF (2001) Novel cannabinoid-sensitive receptor mediates inhibition of glutamatergic synaptic transmission in the hippocampus. Neuroscience 106:1–4
  PubMed CAS Google Scholar
• Hampson RE, Simeral JD, Kelly EJ, Deadwyler SA (2003) Tolerance to the memory disruptive effects of cannabinoids involves adaptation by hippocampal neurons. Hippocampus 13:543–556
  PubMed CAS Google Scholar
• Hart CL, van Gorp W, Haney M, Foltin RW, Fischman MW (2001) Effects of acute smoked marijuana on complex cognitive performance. Neuropsychopharmacology 25:757–765
  PubMed CAS Google Scholar
• Heishman SJ, Huestis MA, Henningfield JE, Cone EJ (1990) Acute and residual effects of marijuana: profiles of plasma THC levels, physiological, subjective, and performance measures. Pharmacol Biochem Behav 37:561–565
  PubMed CAS Google Scholar
• Heishman SJ, Arasteh K, Stitzer ML (1997) Comparative effects of alcohol and marijuana on mood, memory, and performance. Pharmacol Biochem Behav 58:93–101
  PubMed CAS Google Scholar
• Herkenham M, Lynn AB, Little MD, Johnson MR, Melvin LS, de Costa BR, Rice KC (1990) Cannabinoid receptor localization in brain. Proc Natl Acad Sci U S A 87:1932–1936
  PubMed CAS Google Scholar
• 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
  PubMed CAS Google Scholar
• Hoffman AF, Lupica CR (2000) Mechanisms of cannabinoid inhibition of GABA(A) synaptic transmission in the hippocampus. J Neurosci 20:2470–2479
  PubMed CAS Google Scholar
• Hollister LE, Gillespie HK, Ohlsson A, Lindgren JE, Wahlen A, Agurell S (1981) Do plasma concentrations of delta 9-tetrahydrocannabinol reflect the degree of intoxication? J Clin Pharmacol 21:171S–177S
  PubMed CAS Google Scholar
• Hooker WD, Jones RT (1987) Increased susceptibility to memory intrusions and the Stroop interference effect during acute marijuana intoxication. Psychopharmacology (Berl) 91:20–24
  CAS Google Scholar
• Howlett AC (2004) Efficacy in CB1 receptor-mediated signal transduction. Br J Pharmacol 142:1209–1218
  PubMed CAS Google Scholar
• Howlett AC, Barth F, Bonner TI, Cabral G, Casellas P, Devane WA, Felder CC, Herkenham M, Mackie K, Martin BR, Mechoulam R, Pertwee RG (2002) International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol Rev 54:161–202
  PubMed CAS Google Scholar
• Ilan AB, Smith ME, Gevins A (2004) Effects of marijuana on neurophysiological signals of working and episodic memory. Psychopharmacology (Berl) 176:214–222
  CAS Google Scholar
• Iversen L (2003) Comparing cannabis with tobacco: arithmetic does not add up (comment). BMJ 327:165
  PubMed Google Scholar
• Iversen L (2005) Long-term effects of exposure to cannabis. Curr Opin Pharmacol 5:69–72
  PubMed CAS Google Scholar
• Jentsch JD, Verrico CD, Le D, Roth RH (1998) Repeated exposure to delta 9-tetrahydrocannabinol reduces prefrontal cortical dopamine metabolism in the rat. Neurosci Lett 246:169–172
  PubMed CAS Google Scholar
• Johansson E, Agurell S, Hollister LE, Halldin MM (1988) Prolonged apparent half-life of delta 1-tetrahydrocannabinol in plasma of chronic marijuana users. J Pharm Pharmacol 40:374–375
  PubMed CAS Google Scholar
• Kanayama G, Rogowska J, Pope HG, Gruber SA, Yurgelun-Todd DA (2004) Spatial working memory in heavy cannabis users: a functional magnetic resonance imaging study. Psychopharmacology (Berl) 176:239–247
  CAS Google Scholar
• Karniol IG, Carlini EA (1973) Pharmacological interaction between cannabidiol and delta 9-tetrahydrocannabinol. Psychopharmacologia 33:53–70
  PubMed CAS Google Scholar
• Karniol IG, Shirakawa I, Kasinski N, Pfeferman A, Carlini EA (1974) Cannabidiol interferes with the effects of delta 9-tetrahydrocannabinol in man. Eur J Pharmacol 28:172–177
  PubMed CAS Google Scholar
• Karniol IG, Shirakawa I, Takahashi RN, Knobel E, Musty RE (1975) Effects of delta9-tetrahydrocannabinol and cannabinol in man. Pharmacology 13:502–512
  PubMed CAS Google Scholar
• Katona I, Sperlagh B, Magloczky Z, Santha E, Kofalvi A, Czirjak S, Mackie K, Vizi ES, Freund TF (2000) GABAergic interneurons are the targets of cannabinoid actions in the human hippocampus. Neuroscience 100:797–804
  PubMed CAS Google Scholar
• Katona I, Rancz EA, Acsady L, Ledent C, Mackie K, Hajos N, Freund TF (2001) Distribution of CB1 cannabinoid receptors in the amygdala and their role in the control of GABAergic transmission. J Neurosci 21:9506–9518
  PubMed CAS Google Scholar
• Kelly TH, Foltin RW, Rose AJ, Fischman MW, Brady JV (1990) Smoked marijuana effects on tobacco cigarette smoking behavior. J Pharmacol Exp Ther 252:934–944
  PubMed CAS Google Scholar
• Lane SD, Cherek DR, Lieving LM, Tcheremissine OV (2005) Marijuana effects on human forgetting functions. J Exp Anal Behav 83:67–83
  PubMed Google Scholar
• Lichtman AH (2000) SR 141716A enhances spatial memory as assessed in a radial-arm maze task in rats. Eur J Pharmacol 404:175–179
  PubMed CAS Google Scholar
• Lichtman AH, Varvel SA, Martin BR (2002) Endocannabinoids in cognition and dependence. Prostaglandins Leukot Essent Fatty Acids 66:269–285
  PubMed CAS Google Scholar
• Maccarrone M, Valverde O, Barbaccia ML, Castane A, Maldonado R, Ledent C, Parmentier M, Finazzi-Agro A (2002) Age-related changes of anandamide metabolism in CB1 cannabinoid receptor knockout mice: correlation with behaviour. Eur J Neurosci 15:1178–1186
  PubMed Google Scholar
• Mailleux P, Vanderhaeghen JJ (1992) Distribution of neuronal cannabinoid receptor in the adult rat brain: a comparative receptor binding radioautography and in situ hybridization histochemistry. Neuroscience 48:655–668
  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
  PubMed CAS Google Scholar
• Margulies JE, Hammer RP Jr (1991) Delta 9-tetrahydrocannabinol alters cerebral metabolism in a biphasic, dose-dependent manner in rat brain. Eur J Pharmacol 202:373–378
  PubMed CAS Google Scholar
• Marsicano G, Wotjak CT, Azad SC, Bisogno T, Rammes G, Cascio MG, Hermann H, Tang J, Hofmann C, Zieglgansberger W, Di Marzo V, Lutz B (2002) The endogenous cannabinoid system controls extinction of aversive memories (see comment). Nature 418:530–534
  PubMed CAS Google Scholar
• Martin PD, Shapiro ML (2000) Disparate effects of long-term potentiation on evoked potentials and single CA1 neurons in the hippocampus of anesthetized rats. Hippocampus 10:207–212
  PubMed CAS Google Scholar
• Matsuda LA (1997) Molecular aspects of cannabinoid receptors. Crit Rev Neurobiol 11:143–166
  PubMed CAS Google Scholar
• Matsuda LA, Lolait SJ, Brownstein MJ, Young AC, Bonner TI (1990) Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346:561–564
  PubMed CAS Google Scholar
• McGilveray IJ (2005) Pharmacokinetics of cannabinoids. Pain Res Manag 10:15A–22A
  PubMed Google Scholar
• Mechoulam R, Ben-Shabat S, Hanus L, Ligumsky M, Kaminski NE, Schatz AR, Gopher A, Almog S, Martin BR, Compton DR (1995) Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem Pharmacol 50:83–90
  PubMed CAS Google Scholar
• Miller LL, Cornett TL (1978) Marijuana: dose effects on pulse rate, subjective estimates of intoxication, free recall and recognition memory. Pharmacol Biochem Behav 9:573–577
  PubMed CAS Google Scholar
• Miller LL, Cornett T, Brightwell D, McFarland D, Drew WG, Wikler A (1976) Marijuana and memory impairment: the effect of retrieval cues on free recall. Pharmacol Biochem Behav 5:639–643
  PubMed CAS Google Scholar
• Miller LL, Cornett T, Drew W, McFarland D, Brightwell D, Wikler A (1977a) Marijuana: dose–response effects on pulse rate, subjective estimates of potency, pleasantness, and recognition memory. Pharmacology 15:268–275
  Article PubMed CAS Google Scholar
• Miller LL, Cornett TL, Brightwell DR, McFarland DJ, Drew WG, Wikler A (1977b) Marijuana: effects on storage and retrieval of prose material. Psychopharmacology (Berl) 51:311–316
  CAS Google Scholar
• Miller LL, McFarland D, Cornett TL, Brightwell D (1977c) Marijuana and memory impairment: effect on free recall and recognition memory. Pharmacol Biochem Behav 7:99–103
  PubMed CAS Google Scholar
• Miller LL, McFarland DJ, Cornett TL, Brightwell DR, Wikler A (1977d) Marijuana: effects on free recall and subjective organization of pictures and words. Psychopharmacology (Berl) 55:257–262
  CAS Google Scholar
• Miller LL, Cornett T, Nallan G (1978) Marijuana: effect on nonverbal free recall as a function of field dependence. Psychopharmacology (Berl) 58:297–301
  CAS Google Scholar
• Miller LL, Cornett TL, Wikler A (1979) Marijuana: effects on pulse rate, subjective estimates of intoxication and multiple measures of memory. Life Sci 25:1325–1330
  PubMed CAS Google Scholar
• Misner DL, Sullivan JM (1999) Mechanism of cannabinoid effects on long-term potentiation and depression in hippocampal CA1 neurons. J Neurosci 19:6795–6805
  PubMed CAS Google Scholar
• Moscovitch M (1995) Recovered consciousness: a hypothesis concerning modularity and episodic memory. J Clin Exp Neuropsychol 17:276–290
  PubMed CAS Google Scholar
• Munro S, Thomas KL, Abu-Shaar M (1993) Molecular characterization of a peripheral receptor for cannabinoids. Nature 365:61–65
  PubMed CAS Google Scholar
• Nava F, Carta G, Colombo G, Gessa GL (2001) Effects of chronic Delta(9)-tetrahydrocannabinol treatment on hippocampal extracellular acetylcholine concentration and alternation performance in the T-maze. Neuropharmacology 41:392–399
  PubMed CAS Google Scholar
• 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
  PubMed CAS Google Scholar
• Ohlsson A, Lindgren JE, Wahlen A, Agurell S, Hollister LE, Gillespie HK (1980) Plasma delta-9 tetrahydrocannabinol concentrations and clinical effects after oral and intravenous administration and smoking. Clin Pharmacol Ther 28:409–416
  Article PubMed CAS Google Scholar
• Ohlsson A, Lindgren JE, Wahlen A, Agurell S, Hollister LE, Gillespie HK (1981) Plasma levels of delta 9-tetrahydrocannabinol after intravenous, oral, and smoke administration. NIDA Res Monogr 34:250–256
  PubMed CAS Google Scholar
• Owen AM, McMillan KM, Laird AR, Bullmore E (2005) N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies. Hum Brain Mapp 25:46–59
  PubMed Google Scholar
• Pfefferbaum A, Darley CF, Tinklenberg JR, Roth WT, Kopell BS (1977) Marijuana and memory intrusions. J Nerv Ment Dis 165:381–386
  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
  PubMed CAS Google Scholar
• Reibaud M, Obinu MC, Ledent C, Parmentier M, Bohme GA, Imperato A (1999) Enhancement of memory in cannabinoid CB1 receptor knock-out mice. Eur J Pharmacol 379:R1–R2
  PubMed CAS Google Scholar
• Rodriguez de Fonseca F, Del Arco I, Bermudez-Silva FJ, Bilbao A, Cippitelli A, Navarro M (2005) The endocannabinoid system: physiology and pharmacology. Alcohol 40:2–14
  CAS Google Scholar
• Shen M, Thayer SA (1999) Delta9-tetrahydrocannabinol acts as a partial agonist to modulate glutamatergic synaptic transmission between rat hippocampal neurons in culture. Mol Pharmacol 55:8–13
  PubMed CAS Google Scholar
• Shen M, Piser TM, Seybold VS, Thayer SA (1996) Cannabinoid receptor agonists inhibit glutamatergic synaptic transmission in rat hippocampal cultures. J Neurosci 16:4322–4334
  PubMed CAS Google Scholar
• Spencer KM, Nestor PG, Niznikiewicz MA, Salisbury DF, Shenton ME, McCarley RW (2003) Abnormal neural synchrony in schizophrenia. J Neurosci 23:7407–7411
  PubMed CAS Google Scholar
• Squire LR, Alvarez P (1995) Retrograde amnesia and memory consolidation: a neurobiological perspective. Curr Opin Neurobiol 5:169–177
  PubMed CAS Google Scholar
• Stella N, Schweitzer P, Piomelli D (1997) A second endogenous cannabinoid that modulates long-term potentiation. Nature 388:773–778
  PubMed CAS Google Scholar
• Sternberg S (1966) High-speed scanning in human memory. Science 153:652–654
  PubMed CAS Google Scholar
• Stout JC, Murray LL (2001) Assessment of memory in neurogenic communication disorders. Semin Speech Lang 22:137–145
  PubMed CAS Google Scholar
• Sullivan JM (1999) Mechanisms of cannabinoid-receptor-mediated inhibition of synaptic transmission in cultured hippocampal pyramidal neurons. J Neurophysiol 82:1286–1294
  PubMed CAS Google Scholar
• Sullivan JM (2000) Cellular and molecular mechanisms underlying learning and memory impairments produced by cannabinoids. Learn Mem 7:132–139
  PubMed CAS Google Scholar
• Suzuki A, Josselyn SA, Frankland PW, Masushige S, Silva AJ, Kida S (2004) Memory reconsolidation and extinction have distinct temporal and biochemical signatures. J Neurosci 24:4787–4795
  PubMed CAS Google Scholar
• Tanda G, Goldberg SR (2003) Cannabinoids: reward, dependence, and underlying neurochemical mechanisms—a review of recent preclinical data. Psychopharmacology (Berl) 169:115–134
  CAS Google Scholar
• Terranova JP, Michaud JC, Le Fur G, Soubrie P (1995) Inhibition of long-term potentiation in rat hippocampal slices by anandamide and WIN55212-2: reversal by SR141716 A, a selective antagonist of CB1 cannabinoid receptors. Naunyn Schmiedebergs Arch Pharmacol 352:576–579
  PubMed CAS Google Scholar
• Terranova JP, Storme JJ, Lafon N, Perio A, Rinaldi-Carmona M, Le Fur G, Soubrie P (1996) Improvement of memory in rodents by the selective CB1 cannabinoid receptor antagonist, SR 141716. Psychopharmacology 126:165–172
  PubMed CAS Google Scholar
• Tinklenberg JR, Melges FT, Hollister LE, Gillespie HK (1970) Marijuana and immediate memory. Nature 226:1171–1172
  PubMed CAS Google Scholar
• Tinklenberg JR, Kopell BS, Melges FT, Hollister LE (1972) Marihuana and alcohol, Time production and memory functions. Arch Gen Psychiatry 27:812–815
  PubMed CAS Google Scholar
• Tsou K, Brown S, Sanudo-Pena MC, Mackie K, Walker JM (1998) Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83:393–411
  PubMed CAS Google Scholar
• Tulving E (1972) Episodic and semantic memory. Academic Press, New York
  Google Scholar
• Tulving E, Markowitsch HJ (1998) Episodic and declarative memory: role of the hippocampus. Hippocampus 8:198–204
  PubMed CAS Google Scholar
• Turner CE, Elsohly MA, Boeren EG (1980) Constituents of Cannabis sativa L. XVII. A review of the natural constituents. J Nat Prod 43:169–234
  PubMed CAS Google Scholar
• Vachon L, Sulkowski A, Rich E (1974) Marihuana effects on learning, attention and time estimation. Psychopharmacologia 39:1–11
  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
  PubMed Google Scholar
• Varvel SA, Lichtman AH (2002) Evaluation of CB1 receptor knockout mice in the Morris water maze. J Pharmacol Exp Ther 301:915–924
  PubMed CAS Google Scholar
• Varvel SA, Anum EA, Lichtman AH (2005) Disruption of CB(1) receptor signaling impairs extinction of spatial memory in mice. Psychopharmacology (Berl) 179:863–872
  CAS Google Scholar
• Wilson RI, Nicoll RA (2002) Endocannabinoid signaling in the brain. Science 296:678–682
  PubMed CAS Google Scholar
• Wilson WH, Ellinwood EH, Mathew RJ, Johnson K (1994) Effects of marijuana on performance of a computerized cognitive–neuromotor test battery. Psychiatry Res 51:115–125
  PubMed CAS Google Scholar
• Winsauer PJ, Lambert P, Moerschbaecher JM (1999) Cannabinoid ligands and their effects on learning and performance in rhesus monkeys. Behav Pharmacol 10:497–511
  Article PubMed CAS Google Scholar
• Witkin HA, Oltman PK (1967) Cognitive style. Int J Neurol 6:119–137
  Google Scholar
• Wolff MC, Leander JD (2003) SR141716A, a cannabinoid CB1 receptor antagonist, improves memory in a delayed radial maze task. Eur J Pharmacol 477:213–217
  PubMed CAS Google Scholar
• Zimmerberg B, Glick SD, Jarvik ME (1971) Impairment of recent memory by marihuana and THC in rhesus monkeys. Nature 233:343–345
  PubMed CAS Google Scholar