Effects of endocannabinoid system modulation on cognitive and emotional behavior

Frontiers in Behavioral Neuroscience

Volumn , Issue SEPTEMBER, 2011, Pages

  Zanettini, Claudio ^a   Panlilio, Leigh V ^a   Alicki, Mano ^b   Goldberg, Steven R ^a   Haller, József ^b   Yasar, Sevil ^c  

^a NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Animal models; Anxiety; Cognition; Depression; Endocannabinoids; Learning; Memory

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 4 (1,1 DIMETHYLHEPTYL) 1',2',3',4',5',6' HEXAHYDRO 2,3' DIHYDROXY 6' (3 HYDROXYPROPYL)BIPHENYL; 7 PHENYL 1 [5 (2 PYRIDINYL) 2 OXAZOLYL] 1 HEPTANONE; ANANDAMIDE; CANNABIDIOL; CANNABINOID 1 RECEPTOR AGONIST; CANNABINOID 1 RECEPTOR ANTAGONIST; CANNABINOID RECEPTOR; CANNABINOID RECEPTOR AGONIST; CANNABINOID RECEPTOR ANTAGONIST; CANNABIS; CYCLOHEXYLCARBAMIC ACID 3' CARBAMOYLBIPHENYL 3 YL ESTER; DEXANABINOL; DRONABINOL; ENDOCANNABINOID; FATTY ACID AMIDASE; N (4 HYDROXYPHENYL)ARACHIDONAMIDE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PIRINIXIC ACID; RIMONABANT;

ANXIETY; ARTICLE; BEHAVIOR; BRAIN FUNCTION; COGNITION; DEPRESSION; EMOTION; ENVIRONMENTAL FACTOR; ENZYME INHIBITION; FEAR; FORCED SWIMMING TEST; GENE DISRUPTION; HUMAN; LEARNING; LOCOMOTION; LONG TERM MEMORY; MAZE TEST; MEMORY; MEMORY CONSOLIDATION; NEUROTRANSMISSION; NOCICEPTION; NONHUMAN; PASSIVE AVOIDANCE; PROTEIN FUNCTION; RECALL; RECOGNITION; SIGNAL TRANSDUCTION; SPATIAL MEMORY; STIMULUS RESPONSE; TASK PERFORMANCE; WORKING MEMORY;

EID: 84855502083     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2011.00057     Document Type: Article

References (153)

1. Acheson, S. K., Moore, N. L. T., Kuhn, C. M., Wilson, W. A., and Swartzwelder, H. S. (2011). The synthetic cannabinoid WIN 55212-2 differentially modulates thigmotaxis but not spatial learning in adolescent and adult animals. Neurosci. Lett. 487, 411-414.
2. Adamczyk, P., Golda, A., McCreary, A. C., Filip, M., and Przegalin-ski, E. (2008). Activation of endo-cannabinoid transmission induces antidepressant-like effects in rats. J. Physiol. Pharmacol. 59, 217-228.
3. Adermark, L., and Lovinger, D. M. (2007). Retrograde endocannabi-noid signaling at striatal synapses requires a regulated postsynaptic release step. Proc. Natl. Acad. Sci. U.S.A. 104, 20564-20569.
4. Ainge, J. A., Heron-Maxwell, C., The-ofilas, P., Wright, P., de Hoz, L., and Wood, E. R. (2006). The role of the hippocampus in object recognition in rats: examination of the influence of task parameters and lesion size. Behav. Brain Res. 167, 183-195.
5. Bambico, F. R., Cassano, T., Dominguez-Lopez, S., Katz, N., Walker, C. D., Piomelli, D., and Gobbi, G. (2010). Genetic deletion of fatty acid amide hydrolase alters emotional behavior and serotonergic transmission in the dorsal raphe, prefrontal cortex, and hippocampus. Neuropsychopharmacology 35, 2083-2100.
6. Bambico, F. R., Duranti, A., Tontini, A., Tarzia, G., and Gobbi, G. (2009). Endocannabinoids in the treatment of mood disorders: evidence from animal models. Curr. Pharm. Des. 15, 1623-1646.
7. Barna, I., Soproni, K., Arszovszki, A., Csabai, K., and Haller, J. (2007). WIN-55,212-2 chronically implanted into the CA3 region of the dorsal hippocampus impairs learning: a novel method for studying chronic, brain-area-specific effects of cannabinoids. Behav. Pharmacol. 18, 515-520.
8. Beinfeld, M. C., and Connolly, K. (2001). Activation of CB1 cannabi-noid receptors in rat hippocampal slices inhibits potassium-evoked cholecystokinin release, a possible mechanism contributing to the spatial memory defects produced by cannabinoids. Neurosci. Lett. 301, 69-71.
9. Bitencourt, R. M., Pamplona, F. A., and Takahashi, R. N. (2008). Facilitation of contextual fear memory extinction and anti-anxiogenic effects of AM404 and cannabidiol in conditioned rats. Eur. Neuropsychopharmacol. 18, 849-859.
10. Bortolato, M., Mangieri, R. A., Fu, J., Kim, J. H., Arguello, O., Duranti, A., Tontini, A., Mor, M., Tarzia, G., and Piomelli, D. (2007). Antidepressant-like activity of the fatty acid amide hydrolase inhibitor URB597 in a rat model of chronic mild stress. Biol. Psychiatry 62, 1103-1110.
11. Cadogan, A. K., Alexander, S. P., Boyd, E. A., and Kendall, D. A. (1997). Influence of cannabinoids on electrically evoked dopamine release and cyclic AMP generation in the rat striatum. J. Neurochem. 69, 1131-1137.
12. Campolongo, P., Roozendaal, B., Trezza, V., Cuomo, V., Astarita, G., Fu, J., McGaugh, J. L., and Piomelli, D. (2009a). Fat-induced satiety factor oleoylethanolamide enhances memory consolidation. Proc. Natl. Acad. Sci. U.S.A. 106, 8027-8031.
13. Campolongo, P., Roozendaal, B., Trezza, V., Hauer, D., Schelling, G., McGaugh, J. L., and Cuomo, V. (2009b). Endocannabinoids in the rat basolateral amygdala enhance memory consolidation and enable glucocorticoid modulation of memory. Proc. Natl. Acad. Sci. U.S.A. 106, 4888-4893.
14. Cannich, A., Wotjak, C. T., Kamprath, K., Hermann, H., Lutz, B., and Mar-sicano, G. (2004). CB1 cannabinoid receptors modulate kinase and phosphatase activity during extinction of conditioned fear in mice. Learn. Mem. 11, 625-632.
15. Cassano, T., Gaetani, S., Macheda, T., Laconca, L., Romano, A., Morgese, M. G., Cimmino, C. S., Chiarotti, F., Bambico, F. R., Gobbi, G., Cuomo, V., and Piomelli, D. (2011). Evaluation of the emotional phenotype and serotonergic neurotransmission of fatty acid amide hydrolase-deficient mice. Psychopharmacology (Berl.) 214, 465-476.
16. Castellano, C., Cabib, S., Palmisano, A., Di Marzo, V., and Puglisi-Allegra, S. DaSilva, G. E. contributor, and Takahashi, R. N. (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.
17. De Petrocellis, L., and Di Marzo, V. (2010). Non-CB1, non-CB2 receptors for endocannabinoids, plant cannabinoids, and synthetic cannabimimetics: focus on G-protein-coupled receptors and transient receptor potential channels. J. Neuroimmune Pharmacol. 5, 103-121.
18. Deadwyler, S. A., Bunn, T., and Hamp-son, R. E. (1996). Hippocampal ensemble activity during spatial delayed-nonmatch-to-sample performance in rats. J. Neurosci.16, 354-372.
19. Deadwyler, S. A., Goonawardena, A. V., and Hampson, R. E. (2007). Short-term memory is modulated by the spontaneous release of endocannabinoids: evidence from hippocampal population codes. Behav. Pharmacol. 18, 571-580.
20. Deadwyler, S. A., and Hampson, R. E. (2008). Endocannabinoids modulate encoding of sequential memory in the rat hippocampus. Psychopharmacology (Berl.) 198, 577-586.
21. Degroot, A., and Nomikos, G. G. (2004). Genetic deletion and pharmacologi-cal blockade of CB1 receptors modulates anxiety in the shock-probe burying test. Eur. J. Neurosci. 20, 1059-1064.
22. Di Marzo, V., Breivogel, C. S., Tao, Q., Bridgen, D. T., Razdan, R. K., Zim-mer, A. M., Zimmer, A., and Mar-tin, B. R. (2000). Levels, metabolism, and pharmacological activity of anandamide in CB1 cannabinoid receptor knockout mice: evidence for non-CB1, non-CB receptormediated actions of anandamide in mouse brain. J. Neurochem. 75, 2434-2444.
23. Di Marzo, V., De Petrocellis, L., Bisogno, T., and Melck, D. (1999). Metabolism of anandamide and 2-arachidonoylglycerol: an historical overview and some recent developments. Lipids 34(Suppl.), S319-S325.
24. Diana, G., Malloni, M., and Pieri, M. (2003). Effects of the synthetic cannabinoid nabilone on spatial learning and hippocampal neuro-transmission. Pharmacol. Biochem. Behav. 75, 585-591.
25. Egashira, N., Ishigami, N., Mishima, K., Iwasaki, K., Oishi, R., and Fujiwara, M. (2008). Delta9-tetrahydrocannabinol-induced cognitive deficits are reversed by olanzapine but not haloperidol in rats. Prog. Neuropsychopharmacol. Biol. Psychiatry 32, 499-506.
26. Egashira, N., Mishima, K., Iwasaki, K., and Fujiwara, M. (2002). Intrac-erebral microinjections of delta 9-tetrahydrocannabinol: search for the impairment of spatial memory in the eight-arm radial maze in rats. Brain Res. 952, 239-245.
27. ′-carbamoyl-biphenyl-3-yl ester (URB597): effects on anandamide and oleoylethanolamide deactivation. J. Pharmacol. Exp. Ther. 313, 352-358.
28. Fernández-Ruiz, J., Hernández, M., and Ramos, J. A. (2010). Cannabinoid-dopamine interaction in the patho-physiology and treatment of CNS disorders. CNS Neurosci. Ther. 16, e72-e91.
29. Ferrari, F., Ottani, A., Vivoli, R., and Giuliani, D. (1999). Learning impairment produced in rats by the cannabinoid agonist HU 210 in a water-maze task. Pharmacol. Biochem. Behav. 64, 555-561.
30. Fride, E., Suris, R., Weidenfeld, J., and Mechoulam, R. (2005). Differential response to acute and repeated stress in cannabinoid CB1 receptor knock-out newborn and adult mice. Behav. Pharmacol. 16, 431-440.
31. Ganon-Elazar, E., and Akirav, I. (2009). Cannabinoid receptor activation in the basolateral amygdala blocks the effects of stress on the conditioning and extinction of inhibitory avoidance. J. Neurosci. 29, 11078-11088.
32. Gerdeman, G., and Lovinger, D. M. (2001). CB1 cannabinoid receptor inhibits synaptic release of glutamate in rat dorsolateral striatum. J. Neurophysiol. 85, 468-471.
33. Gifford, A. N., and Ashby, C. R. Jr. (1996). Electrically evoked acetyl-choline release from hippocampal slices is inhibited by the cannabinoid receptor agonist, WIN 55212-2, and is potentiated by the cannabinoid antagonist, SR 141716A. J. Pharma-col. Exp. Ther. 277, 1431-1436.
34. Gobbi, G., Bambico, F. R., Mangieri, R., Bortolato, M., Campolongo, P., Soli-nas, M., Cassano, T., Morgese, M. G., Debonnel, G., Duranti, A., Ton-tini, A., Tarzia, G., Mor, M., Trezza, V., Goldberg, S. R., Cuomo, V., and Piomelli, D. (2005). Antidepressant-like activity and modulation of brain monoaminergic transmission by blockade of anandamide hydrolysis. Proc. Natl. Acad. Sci. U.S.A. 102, 18620-18625.
35. Goonawardena, A. V., Robinson, L., Hampson, R. E., and Riedel, G. (2010). Cannabinoid and cholinergic systems interact during performance of a short-term memory task in the rat. Learn. Mem. 28, 502-211.
36. Griebel, G., Stemmelin, J., and Scatton, B. (2005). Effects of the cannabinoid CB1 receptor antagonist rimonabant in models of emotional reactivity in rodents. Biol. Psychiatry 57, 261-267.
37. Hájos, N., and Freund, T. F. (2002). Pharmacological separation of cannabinoid sensitive receptors on hippocampal excitatory and inhibitory fibers. Neuropharmacology 43, 503-510.
38. Haller, J., Bakos, N., Szirmay, M., Ledent, C., and Freund, T. F. (2002). The effects of genetic and pharmacological blockade of the CB1 cannabinoid receptor on anxiety. Eur. J. Neurosci. 16, 1395-1398.
39. Haller, J., Barna, I., Barsvari, B., Gyimesi Pelczer, K., Yasar, S., Panlilio, L. V., and Goldberg, S. (2009). Interactions between environmental aversiveness and the anxiolytic effects of enhanced cannabinoid signaling by FAAH inhibition in rats. Psychophar-macology (Berl.) 204, 607-616.
40. Haller, J., Mátyás, F., Soproni, K., Varga, B., Barsy, B., Németh, B., Mikics, E., Freund, T. F., and Hájos, N. (2007). Correlated species differences in the effects of cannabinoid ligands on anxiety and on GABAergic and glutamatergic synaptic transmission. Eur. J. Neurosci. 25, 2445-2456.
41. Haller, J., Varga, B., Ledent, C., Barna, I., and Freund, T. F. (2004a). Context-dependent effects of CB1 cannabi-noid gene disruption on anxiety-like and social behaviour in mice. Eur. J. Neurosci. 19, 1906-1912.
42. Haller, J., Varga, B., Ledent, C., and Fre-und, T. F. (2004b). CB1 cannabi-noid receptors mediate anxiolytic effects: convergent genetic and pharmacological evidence with CB1-specific agents. Behav. Pharmacol. 15, 299-304.
43. Hampson, R. E., and Deadwyler, S. A. (2000). Cannabinoids reveal the necessity of hippocampal neural encoding for short-term memory in rats. J. Neurosci. 20, 8932-8942.
44. Harloe, J. P., Thorpe, A. J., and Lichtman, A. H. (2008). Differential endocannabinoid regulation of extinction in appetitive and aversive Barnes maze tasks. Learn. Mem. 15, 806-809.
45. Herkenham, M., Lynn, A. B., Johnson, M. R., Melvin, L. S., de Costa, B. R., and Rice, K. C. (1991). Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J. Neurosci. 11, 563-583.
46. Heuer, E., and Bachevalier, J. (2011). Effects of selective neonatal hip-pocampal lesions on tests of object and spatial recognition memory in monkeys. Behav. Neurosci. 125, 137-149.
47. Heyser, C. J., Hampson, R. E., and Dead-wyler, S. A. (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.
48. Hill, M. N., Froese, L. M., Morrish, A. C., Sun, J. C., and Floresco, S. B. (2006). Alterations in behavioral flexibility by cannabinoid CB1 receptor agonists and antagonists. Psychophar-macology (Berl.) 187, 245-259.
49. Hill, M. N., Hillard, C. J., and McEwen, B. S. (2011). Alterations in corticolimbic dendritic morphology and emotional behavior in cannabinoid CB1 receptor-deficient parallel the effects of chronic stress. Cereb. Cortex 21, 2056-2064.
50. Hill, M. N., Karacabeyli, E. S., and Gorzalka, B. B. (2007). Estro-gen recruits the endocannabinoid system to modulate emotionality. Psychoneuroendocrinology 32, 350-357.
51. Hohmann, A. G., Suplita, R. L., Bolton, N. M., Neely, M. H., Fegley, D., Mangieri, R., Krey, J. F., Walker, J. M., Holmes, P. V., Crystal, J. D., Duranti, A., Tontini, A., Mor, M., Tarzia, G., and Piomelli, D. (2005). An endocannabinoid mechanism for stress-induced analgesia. Nature 435, 1108-1112.
52. Hölter, S. M., Kallnik, M., Wurst, W., Marsicano, G., Lutz, B., and Wot-jak, C. T. (2005). Cannabinoid CB1 receptor is dispensable for memory extinction in an appetitively-motivated learning task. Eur. J. Phar-macol. 510, 69-74.
53. Houchi, H., Babovic, D., Pierrefiche, O., Ledent, C., Daoust, M., and Naassila, M. (2005). CB1 receptor knockout display reduced ethanol-induced conditioned place preference and increased striatal dopamine D2 receptors. Neuropsychopharmacology 30, 339-349.
54. Inui, K., Egashira, N., Mishima, K., Yano, A., Matsumoto, Y., Hasebe, N., Abe, K., Hayakawa, K., Ikeda, T., Iwasaki, K., and Fujiwara, M. (2004). The serotonin1A receptor agonist 8-OHDPAT reverses delta 9-tetrahydrocannabinol-induced impairment of spatial memory and reduction of acetylcholine release in the dorsal hippocampus in rats. Neurotox. Res. 6, 153-158.
55. Isaacson, R. L., and Wickelgren, W. O. (1962). Hippocampal ablation and passive avoidance. Science 138, 1104-1106.
56. Ishac, E. J., Jiang, L., Lake, K. D., Varga, K., Abood, M. E., and Kunos, G. (1996). Inhibition of exocytotic noradrenaline release by presynaptic cannabinoid CB1 receptors on peripheral sympathetic nerves. Br. J. Pharmacol. 118, 2023-2028.
57. Jacob, W., Yassouridis, A., Marsicano, G., Monory, K., Lutz, B., and Wot-jak, C. T. (2009). Endocannabinoids render exploratory behaviour largely independent of the test aversiveness: role of glutamatergic transmission. Genes Brain Behav. 8, 685-698.
58. Jentsch, J. D., Verrico, C. D., Le, D., and Roth, R. H. (1998). Repeated exposure to delta-9-tetrahydrocannabinol reduces prefrontal cortical dopamine metabolism in the rat. Neurosci. Lett. 246, 169-172.
59. Kamprath, K., Marsicano, G., Tang, J., Monory, K., Bisogno, T., Di Marzo, V., Lutz, B., and Wotjak, C. T. (2006). Cannabinoid CB1 receptor mediates fear extinction via habituation-like processes. J. Neurosci. 26, 6677-6686.
60. Kathuria, S., Gaetani, S., Fegley, D., Valiño, F., Duranti, A., Tontini, A., Mor, M., Tarzia, G., La Rana, G., Calignano, A., Giustino, A., Tattoli, M., Palmery, M., Cuomo, V., and Piomelli, D. (2003). Modulation of anxiety through blockade of anandamide hydrolysis. Nat. Med. 9, 76-81.
61. Katona, I., and Freund, T. F. (2008). Endocannabinoid signaling as a synaptic circuit breaker in neurological disease. Nat. Med. 14, 923-930.
62. Katona, I., Rancz, E. A., Acsady, L., Ledent, C., Mackie, K., Hajos, N., and Freund, T. F. (2001). Distribution of CB1 cannabinoid receptors in the amygdala and their role in the control of GABAer-gic transmission. J. Neurosci. 21, 9506-9518.
63. Katona, I., Sperlágh, B., Sík, A., Käfalvi, A., Vizi, E. S., Mackie, K., and Freund, T. F. (1999). Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J. Neurosci. 19, 4544-4558.
64. Kawamura, Y., Fukaya, M., Maejima, T., Yoshida, T., Miura, E., Watanabe, M., Ohno-Shosaku, T., and Kano, M. (2006). The CB1 cannabinoid receptor is the major cannabinoid receptor at excitatory presynaptic sites in the hippocampus and cerebellum. J. Neurosci. 26, 2991-3001.
65. Kirkham, T. C., Williams, C. M., Fezza, F., and Di Marzo, V. (2002). Endo-cannabinoid levels in rat limbic fore-brain and hypothalamus in relation to fasting, feeding and satiation: stimulation of eating by 2-arachidonoyl glycerol. Br. J. Pharma-col. 136, 550-557.
66. Lau, T., and Schloss, P. (2008). The cannabinoid CB1 receptor is expressed on serotonergic and dopaminergic neurons. Eur. J. Pharmacol. 578, 137-141.
67. Lichtman, A. H. (2000). SR 141716A enhances spatial memory as assessed in a radial-arm maze task in rats. Eur. J. Pharmacol. 404, 175-179.
68. Lichtman, A. H., Dimen, K. R., and Martin, B. R. (1995). Systemic or intrahippocampal cannabi-noid administration impairs spatial memory in rats. Psychopharmacol-ogy (Berl.) 119, 282-290.
69. Lichtman, A. H., and Martin, B. R. (1996). Delta 9-tetrahydrocannabinol impairs spatial memory through a cannabinoid receptor mechanism. Psychopharmacology (Berl.) 126, 125-131.
70. Lisboa, S. F., Resstel, L. B. M., Aguiar, D. C., and Guimarães, F. S. (2008). Activation of cannabinoid CB1 receptors in the dorsolateral periaqueductal gray induces anxiolytic effects in rats submitted to the Vogel conflict test. Eur. J. Pharmacol. 593, 73-78.
71. Long, J. Z., Li, W., Booker, L., Burston, J. J., Kinsey, S. G., Schlosburg, J. E., Pavón, F. J., Serrano, A. M., Selley, D. E., Parsons, L. H., Lichtman, A. H., and Cravatt, B. F. (2009). Selective blockade of 2-arachidonoylglycerol hydrolysis produces cannabinoid behavioral effects. Nat. Chem. Biol. 5, 37-44.
72. Lutz, B. (2004). On-demand activation of the endocannabinoid system in the control of neuronal excitability and epileptiform seizures. Biochem. Pharmacol. 68, 1691-1698.
73. Maccarrone, M., Valverde, O., Barbaccia, M. L., Castañé, A., Maldonado, R., Ledent, C., Parmentier, M., and Finazzi-Agrò, A. (2002). Age-related changes of anandamide metabolism in CB1 cannabinoid receptor knock-out mice: correlation with behaviour. Eur. J. Neurosci. 15, 1178-1186.
74. Mallet, P. E., and Beninger, R. J. (1998). The cannabinoid CB1 receptor antagonist SR141716A attenuates the memory impairment produced by delta9-tetrahydrocannabinol or anandamide. Psychopharmacology (Berl.) 140, 11-19.
75. Manna, S. S. S., and Jain, N. S. (2011). Involvement of endo-cannabinoids in antidepressant and anti-compulsive effect of fluoxetine in mice. Behav. Brain Res. 223, 125-134.
76. Marsicano, G., Goodenough, S., Monory, K., Hermann, H., Eder, M., Cannich, A., Azad, S. C., Cascio, M. G., Gutiérrez, S. O., van der Stelt, M., López-Rodriguez, M. L., Casanova, E., Schütz, G., Zieglgänsberger, W., Di Marzo, V., Behl, C., and Lutz, B. (2003). CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 302, 84-88.
77. Marsicano, G., Wotjak, C. T., Azad, S. C., Bisogno, T., Rammes, G., Cascio, M. G., Hermann, H., Tang, J., Hofmann, C., Zieglgänsberger, W., Di Marzo, V., and Lutz, B. (2002). The endogenous cannabinoid system controls extinction of aversive memories. Nature 418, 530-534.
78. Martin, M., Ledent, C., Parmentier, M., Maldonado, R., and Valverde, O. (2002). Involvement of CB1 cannabinoid receptors in emotional behaviour. Psychopharmacology (Berl.) 159, 379-387.
79. Mascia, P., Pistis, M., Justinova, Z., Panlilio, L. V., Luchicchi, A., Lecca, S., Scherma, M., Fratta, W., Fadda, P., Barnes, C., Redhi, G. H., Yasar, S., Le Foll, B., Tanda, G., Piomelli, D., and Goldberg, S. R. (2011). Blockade of nicotine reward and reinstatement by activation of alpha-type peroxisome proliferator-activated receptors. Biol. Psychiatry 69, 633-641.
80. Mazzola, C., Medalie, J., Scherma, M., Panlilio, L. V., Solinas, M., Tanda, G., Drago, F., Cadet, J. L., Goldberg, S. R., and Yasar, S. (2009). Fatty acid amide hydrolase (FAAH) inhibition enhances memory acquisition through activation of PPAR-alpha nuclear receptors. Learn. Mem. 16, 332-337.
81. McLaughlin, R. J., Hill, M. N., Morrish, A. C., and Gorzalka, B. B. (2007). Local enhancement of cannabinoid CB1 receptor signalling in the dorsal hippocampus elicits an antidepressant-like effect. Behav. Pharmacol. 18, 431-438.
82. Melis, M., Carta, S., Fattore, L., Tolu, S., Yasar, S., Goldberg, S. R., Fratta, W., Maskos, U., and Pistis, M. (2010). Peroxisome proliferator-activated receptors-alpha modulate dopamine cell activity through nicotinic receptors. Biol. Psychiatry 68, 256-264.
83. Micale, V., Cristino, L., Tamburella, A., Petrosino, S., Leggio, G. M., Drago, F., and Di Marzo, V. (2009). Anxiolytic effects in of a dual blocker of fatty acid amide hydrolase and transient receptor potential vanilloid type-1 channels. Neuropsychophar-macology 34, 593-606.
84. Mikics, E., Dombi, T., Barsvári, B., Varga, B., Ledent, C., Freund, T. F., and Haller, J. (2006). The effects of cannabinoids on contextual conditioned fear in CB1 knockout and CD1 mice. Behav. Pharmacol. 17, 223-230.
85. Mikics, E., Vas, J., Aliczki, M., Halasz, J., and Haller, J. (2009). Interactions between the anxiogenic effects of CB1 gene disruption and 5-HT3 neurotransmission. Behav. Pharmacol. 20, 265-272.
86. Millan, M. J. (2003). The neurobiology and control of anxious states. Prog. Neurobiol. 70, 83-244.
87. Mishima, K., Egashira, N., Hirosawa, N., Fujii, M., Matsumoto, Y., Iwasaki, K., and Fujiwara, M. (2001). Characteristics of learning and memory impairment induced by delta9-tetrahydrocannabinol in rats. Jpn. J. Pharmacol. 87, 297-308.
88. Mishima, K., Egashira, N., Matsumoto, Y., Iwasaki, K., and Fujiwara, M. (2002). Involvement of reduced acetylcholine release in delta9-tetrahydrocannabinol-induced impairment of spatial memory in the 8-arm radial maze. Life Sci. 72, 397-407.
89. Moise, A. M., Eisenstein, S. A., Astarita, G., Piomelli, D., and Hohmann, A. G. (2008). An endocannabi-noid signaling system modulates anxiety-like behavior in male Syrian hamsters. Psychopharmacology (Berl.) 200, 333-346.
90. Molina-Holgado, F., Molina-Holgado, E., Leret, M. L., González, M. I., and Reader, T. A. (1993). Distribution of indoleamines and [3H]paroxetine binding in rat brain regions following acute or perinatal delta 9-tetrahydrocannabinol treatments. Neurochem. Res. 18, 1183-1191.
91. Moore, N. L. T., Greenleaf, A. L. R., Acheson, S. K., Wilson, W. A., Swartzwelder, H. S., and Kuhn, C. M. (2010). Role of cannabi-noid receptor type 1 desensitization in greater tetrahydrocannabinol impairment of memory in adolescent rats. J. Pharmacol. Exp. Ther. 335, 294-301.
92. ′-substituted biphenyl-3-yl esters as fatty acid amide hydrolase inhibitors: synthesis, quantitative structure-activity relationships, and molecular mod-eling studies. J. Med. Chem. 47, 4998-5008.
93. Moreira, F. A., Grieb, M., and Lutz, B. (2009). Central side-effects of therapies based on CB1 cannabi-noid receptor agonists and antagonists: focus on anxiety and depression. Best Prac. Res. Clin. Endocrinol. Metab. 23, 133-144.
94. Moreira, F. A., Kaiser, N., Monory, K., and Lutz, B. (2008). Reduced anxiety-like behaviour induced by genetic and pharmacological inhibition of the endocannabinoid-degrading enzyme fatty acid amide hydrolase (FAAH) is mediated by CB1 receptors. Neuropharmacology 54, 141-150.
95. Moreira, F. A., and Wotjak, C. T. (2010). Cannabinoids and anxiety. Curr. Top. Behav. Neurosci. 2, 429-450.
96. Morgese, M. G., Cassano, T., Gae-tani, S., Macheda, T., Laconca, L., Dipasquale, P., Ferraro, L., Antonelli, T., Cuomo, V., and Giuffrida, A. (2009). Neurochemical changes in the striatum of dyskinetic rats after administration of the cannabinoid agonist WIN55,212-2. Neurochem. Int. 54, 56-64.
97. Murillo-Rodríguez, E., Giordano, M., Cabeza, R., Henriksen, S. J., Méndez Díaz, M., Navarro, L., and Prospéro-García, O. (2001). Oleamide modulates memory in rats. Neurosci. Lett. 313, 61-64.
98. Naderi, N., Haghparast, A., SaberTehrani, A., Rezaii, N., Alizadeh, A.-M., Khani, A., and Motamedi, F. (2008). Interaction between cannabinoid compounds and diazepam on anxiety-like behaviour of mice. Pharmacol. Biochem. Behav. 89, 64-75.
99. Naidu, P. S., Varvel, S. A., Ahn, K., Cravatt, B. F., Martin, B. R., and Licht-man, A. H. (2007). Evaluation of fatty acid amide hydrolase inhibition in murine models of emotionality. Psychopharmacology (Berl.) 192, 61-70.
100. Nakamura, E. M., da Silva, E. A., Concilio, G. V., Wilkinson, D. A., and Masur, J. (1991). Reversible effects of acute and long-term administration of delta-9-tetrahydrocannabinol (THC) on memory in the rat. Drug Alcohol Depend. 28, 167-175.
101. Nakazi, M., Bauer, U., Nickel, T., Kathmann, M., and Schlicker, E. (2000). Inhibition of serotonin release in the mouse brain via presynaptic cannabinoid CB1 receptors. Naunyn Schmiedebergs Arch. Pharmacol. 361, 19-24.
102. Nasehi, M., Piri, M., Jamali-Raeufy, N., and Zarrindast, M. R. (2010). Influence of intracerebral administration of NO agents in dorsal hippocampus (CA1) on cannabinoid state-dependent memory in the step-down passive avoidance test. Physiol. Behav. 100, 297-304.
103. Nava, F., Carta, G., Battasi, A. M., and Gessa, G. L. (2000). D dopamine receptors enable delta-tetrahydrocannabinol induced memory impairment and reduction of hippocampal extracellular acetylcholine concentration. Br. J. Pharmacol. 130, 1201-1210.
104. Nava, F., Carta, G., Colombo, G., and Gessa, G. L. (2001). Effects of chronic delta-tetrahydrocannabinol treatment on hippocampal extra-cellular acetylcholine concentration and alternation performance in the T-maze. Neuropharmacology 41, 392-399.
105. Niyuhire, F., Varvel, S. A., Thorpe, A. J., Stokes, R. J., Wiley, J. L., and Licht-man, A. H. (2007). The disruptive effects of the CB1 receptor antagonist rimonabant on extinction learning in are task-specific. Psychophar-macology (Berl.) 191, 223-231.
106. Pamplona, F. A., Bitencourt, R. M., and Takahashi, R. N. (2008). Short-and long-term effects of cannabinoids on the extinction of contextual fear memory in rats. Neurobiol. Learn. Mem. 90, 290-293.
107. Pamplona, F. A., Prediger, R. D., Pandolfo, P., and Takahashi R. N. (2006). The cannabinoid receptor agonist WIN 55,212-2 facilitates the extinction of contextual fear memory and spatial memory in rats. Psychopharmacology (Berl) 188, 641-649.
108. Pamplona, F. A., and Takahashi, R. N. (2006). WIN 55212-2 impairs contextual fear conditioning through the activation of CB1 cannabinoid receptors. Neurosci. Lett. 397, 88-92.
109. Panlilio, L. V., Yasar, S., Thorndike, E. B., Goldberg, S. R., and Schindler, C. W. (2011). Automatic recording of mediating behavior in delayed matching-and nonmatching-to-position procedures in rats. Psychopharmacology (Berl.) 214, 495-504.
110. Patel, S., and Hillard, C. J. (2006). Phar-macological evaluation of cannabi-noid receptor ligands in a mouse model of anxiety: further evidence for an anxiolytic role for endogenous cannabinoid signaling. J. Pharmacol. Exp. Ther. 318, 304-311.
111. Phillips, R. G., and LeDoux, J. E. (1992). Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 106, 274-285.
112. Piomelli, D., Tarzia, G., Duranti, A., Tontini, A., Mor, M., Compton, T. R., Dasse, O., Monaghan, E. P., Parrott, J. A., and Putman, D. (2006). Pharmacological profile of the selective FAAH inhibitor KDS-4103 (URB597). CNS Drug Rev. 12, 21-38.
113. Quinn, H. R., Matsumoto, I., Callaghan, P. D., Long, L. E., Arnold, J. C., Gunasekaran, N., Thompson, M. R., Dawson, B., Mallet, P. E., Kashem, M. A., Matsuda-Matsumoto, H., Iwazaki, T., and McGregor, I. S. (2008). Adolescent rats find repeated delta-THC less aversive than adult rats but display greater residual cognitive deficits and changes in hippocampal protein expression following exposure. Neuropsychopharma-cology 33, 1113-1126.
114. Quirk, G. J., and Mueller, D. (2008). Neural mechanisms of extinction learning and retrieval. Neuropsy-chopharmacology 33, 56-72.
115. Ranganathan, M., and D'Souza, D. C. (2006). The acute effects of cannabi-noids on memory in humans: a review. Psychopharmacology (Berl.) 188, 425-444.
116. Realini, N., Vigano, D., Guidali, C., Zam-berletti, E., Rubino, T., and Parolaro, D. (2011). Chronic URB597 treatment at adulthood reverted most depressive-like symptoms induced by adolescent exposure to THC in female rats. Neuropharmacology 60, 235-243.
117. Riedel, G., and Davies, S. N. (2005). Cannabinoid function in learning, memory and plasticity. Handb. Exp. Pharmacol. 168, 445-477.
118. Robinson, L., Goonawardena, A. V., Pertwee, R., Hampson, R. E., Platt, B., and Riedel, G. (2010). WIN55,212-2 induced deficits in spatial learning are mediated by cholinergic hypo-function. Behav. Brain Res. 208, 584-592.
119. Rodrigues, L. C., de, M., Conti, C. L., and Nakamura-Palacios, E. M. (2011). Clozapine and SCH 23390 prevent the spatial working memory disruption induced by (Δ-THC administration into the medial prefrontal cortex. Brain Res. 1382, 230-237.
120. Rubino, T., Realini, N., Braida, D., Guidi, S., Capurro, V., Viganò, D., Guidali, C., Pinter, M., Sala, M., Bartesaghi, R., and Parolaro, D. (2009). Changes in hippocampal morphology and neuroplasticity induced by adolescent THC treatment are associated with cognitive impairment in adulthood. Hippocampus 19, 763-772.
121. Rubino, T., Realini, N., Castiglioni, C., Guidali, C., Viganó, D., Marras, E., Petrosino, S., Perletti, G., Maccarrone, M., Di Marzo, V., and Parolaro, D. (2008). Role in anxiety behavior of the endocannabinoid system in the prefrontal cortex. Cereb. Cortex 18, 1292-1301.
122. Scherma, M., Medalie, J., Fratta, W., Vadivel, S. K., Makriyannis, A., Piomelli, D., Mikics, E., Haller, J., Yasar, S., Tanda, G., and Goldberg, S. R. (2008). The endogenous cannabinoid anandamide has effects on motivation and anxiety that are revealed by fatty acid amide hydrolase (FAAH) inhibition. Neurophar-macology 54, 129-140.
123. Schneider, M., and Koch, M. (2002). The cannabinoid agonist WIN 55,212-2 reduces sensorimotor gating and recognition memory in rats. Behav. Pharmacol. 13, 29-37.
124. Schneider, M., Schömig, E., and Leweke, F. M. (2008). PRECLIN-ICAL STUDY: acute and chronic cannabinoid treatment differentially affects recognition memory and social behavior in pubertal and adult rats. Addict. Biol. 13, 345-357.
125. Seillier, A., and Giuffrida, A. (2011). Inhibition of fatty acid amide hydrolase modulates anxiety-like behavior in PCP-treated rats. Pharmacol. Biochem. Behav. 98, 583-586.
126. Silva de Melo, L. C., Cruz, A. P., Rios Valentim, S. J. Jr., Marinho, A. R., Mendonça, J. B., and Nakamura-Palacios, E. M. (2005). Delta-THC administered into the medial prefrontal cortex disrupts the spatial working memory. Psychopharmacol-ogy (Berl.) 183, 54-64.
127. Sink, K. S., Segovia, K. N., Collins, L. E., Markus, E. J., Vemuri, V. K., Makriyannis, A., and Salamone, J. D. (2010). The CB1 inverse ago-nist AM251, but not the CB1 antagonist AM4113, enhances retention of contextual fear conditioning in rats. Pharmacol. Biochem. Behav. 95, 479-484.
128. Steiner, M. A., Marsicano, G., Nestler, E. J., Holsboer, F., Lutz, B., and Wotjak, C. T. (2008a). Antidepressant-like behavioral effects of impaired cannabinoid receptor type 1 signal- ing coincide with exaggerated corticosterone secretion in mice. Psy-choneuroendocrinology 33, 54-67.
129. Steiner, M. A., Marsicano, G., Wot-jak, C. T., and Lutz, B. (2008b). Conditional cannabinoid receptor type 1 mutants reveal neuron subpopulation-specific effects on behavioral and neuroendocrine stress responses. Psychoneuroen- docrinology 33, 1165-1170.
130. Straiker, A., and Mackie, K. (2009). Cannabinoid signaling in inhibitory autaptic hippocampal neurons. Neuroscience 163, 190-201.
131. Suenaga, T., and Ichitani, Y. (2008). Effects of hippocampal administration of a cannabinoid receptor agonist WIN 55,212-2 on spontaneous object and place recognition in rats. Behav. Brain Res. 190, 248-252.
132. Suenaga, T., Kaku, M., and Ichitani, Y. (2008). Effects of intrahippocam-pal cannabinoid receptor agonist and antagonist on radial maze and T-maze delayed alternation perfor- mance in rats. Pharmacol. Biochem. Behav. 91, 91-96.
133. Suzuki, A., Josselyn, S. A., Frankland, P. W., Masushige, S., Silva, A. J., and Kida, S. (2004). Memory recon- solidation and extinction have distinct temporal and biochemical sig- natures. J. Neurosci. 24, 4787-4795.
134. Tart, C. T. (1970). Marijuana intoxi-cation common experiences. Nature 226, 701-704.
135. Tarzia, G., Duranti, A., Tontini, A., Piersanti, G., Mor, M., Rivara, S., Plazzi, P. V., Park, C., Kathuria, S., and Piomelli, D. (2003). Design, synthesis, and structure-activity relationships of alkylcarbamic acid aryl esters, a new class of fatty acid amide hydrolase inhibitors. J. Med. Chem. 46, 2352-2360.
136. Terranova, J. P., Storme, J. J., Lafon, N., Pério, A., Rinaldi-Carmona, M., Le Fur, G., Soubrié, P., and Umathe, S. N. (1996). Improvement of memory in rodents by the selective CB1 cannabinoid receptor antagonist, SR 141716. Psychopharmacology (Berl.) 126, 165-172.
137. Umathe, S. N., Manna, S. S., and Jain, N. S. (2011). Involvement of endo-cannabinoids in antidepressant and anti-compulsive effect of fluoxetine in mice. Behav. Brain Res. 223, 125-134.
138. Urigüen, L., Pérez-Rial, S., Ledent, C., Palomo, T., and Manzanares, J. (2004). Impaired action of anxiolytic drugs in deficient in cannabi-noid CB1 receptors. Neuropharma-cology 46, 966-973.
139. Varvel, S. A., Anum, E. A., and Licht-man, A. H. (2005a). Disruption of CB1 receptor signaling impairs extinction of spatial memory in mice. Psychopharmacology (Berl.) 179, 863-872.
140. Varvel, S. A., Anum, E., Niyuhire, F., Wise, L. E., and Lichtman, A. H. (2005b). Delta-THC-induced cognitive deficits in are reversed by the GABA(A) antagonist bicuculline. Psychopharmacology (Berl.) 178, 317-327.
141. Varvel, S. A., Cravatt, B. F., Engram, A. E., and Lichtman, A. H. (2006). Fatty acid amide hydrolase (-/-) exhibit an increased sensitivity to the disruptive effects of anandamide or oleamide in a working memory water maze task. J. Pharmacol. Exp. Ther. 317, 251-257.
142. Varvel, S. A., Hamm, R. J., Martin, B. R., and Lichtman, A. H. (2001). Differential effects of delta 9-THC on spatial reference and working memory in mice. Psychopharmacology (Berl.) 157, 142-150.
143. Varvel, S. A., and Lichtman, A. H. (2002). Evaluation of CB1 recep-tor knockout in the Morris water maze. J. Pharmacol. Exp. Ther. 301, 915-924.
144. Varvel, S. A., Wise, L. E., and Licht-man, A. H. (2009). Are CB1 receptor antagonists nootropic or cognitive impairing agents? Drug Dev. Res. 70, 555-565.
145. Varvel, S. A., Wise, L. E., Niyuhire, F., Cravatt, B. F., and Lichtman, A. H. (2007). Inhibition of fatty-acid amide hydrolase accelerates acquisition and extinction rates in a spatial memory task. Neuropsychopharma-cology 32, 1032-1041.
146. Walker, J. M., Huang, S. M., Strangman, N. M., Tsou, K., and Sañudo-Peña, M. C. (1999). Pain modulation by release of the endogenous cannabi-noid anandamide. Proc. Natl. Acad. Sci. U.S.A. 96, 12198-12203.
147. Wilson, R. I., and Nicoll, R. A. (2001). Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410, 588-592.
148. Wise, L. E., Harloe, J. P., and Licht-man, A. H. (2009a). Fatty acid amide hydrolase (FAAH) knockout exhibit enhanced acquisition of an aversive, but not of an appetitive, Barnes maze task. Neurobiol. Learn. Mem. 92, 597-601.
149. Wise, L. E., Thorpe, A. J., and Licht-man, A. H. (2009b). Hippocampal CB1 receptors mediate the memory impairing effects of delta-tetrahy-drocannabinol. Neuropsychophar-macology 34,2072-2080.
150. Wise, L. E., Iredale, P. A., and Licht-man, A. H. (2008). The cannabi-noid CB1 receptor antagonist CE prolongs spatial memory duration in a rat delayed radial arm maze memory task. Eur. J. Pharmacol. 590, 246-249.
151. Wise, L. E., Iredale, P. A., Stokes, R. J., and Lichtman, A. H. (2007). Combination of rimonabant and donepezil prolongs spatial memory duration. Neuropsychopharmacology 32, 1805-1812.
152. Wolff, M. C., and Leander, J. D. (2003). SR141716A, a cannabinoid CB1 receptor antagonist, improves memory in a delayed radial maze task. Eur. J. Pharmacol. 477, 213-217.
153. Wright, L. K. M., Liu, J., Nallapa-neni, A., and Pope, C. N. (2010). Behavioral sequelae following acute diisopropylfluorophosphate intoxication in rats: comparative effects of atropine and cannabinomimetics. Neurotoxicol. Teratol. 32, 329-335.