Pharmacological elevation of anandamide impairs short-term memory by altering the neurophysiology in the hippocampus

Neuropharmacology

Volumn 61, Issue 5-6, 2011, Pages 1016-1025

  Goonawardena, Anushka V ^a   Sesay, John ^a   Sexton, Cheryl Ann ^a   Riedel, Gernot ^a,b   Hampson, Robert E ^a,b  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Delayed non match to sample; Electrophysiology; Endocannabinoid; Ensemble code; Hippocampus; Short term memory; Single unit recording

Indexed keywords

ANANDAMIDE; CAPSAICIN; CYCLOHEXYLCARBAMIC ACID 3' CARBAMOYLBIPHENYL 3 YL ESTER; ENDOCANNABINOID; FATTY ACID AMIDASE INHIBITOR; METHANANDAMIDE; N (4 HYDROXYPHENYL)ARACHIDONAMIDE; VANILLOID RECEPTOR 1;

ANIMAL EXPERIMENT; ARTICLE; BRAIN FUNCTION; BRAIN NERVE CELL; DRUG MEGADOSE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; LONG EVANS RAT; LOW DRUG DOSE; MALE; MEMORY CONSOLIDATION; MEMORY DISORDER; MENTAL TASK; NONHUMAN; PHARMACOLOGICAL PROCEDURES; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; RAT; SHORT TERM MEMORY; TASK PERFORMANCE;

ACTION POTENTIALS; AMIDOHYDROLASES; ANIMALS; ARACHIDONIC ACIDS; BEHAVIOR, ANIMAL; CA1 REGION, HIPPOCAMPAL; CA3 REGION, HIPPOCAMPAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG EVALUATION, PRECLINICAL; ELECTROPHYSIOLOGICAL PHENOMENA; ENDOCANNABINOIDS; HIPPOCAMPUS; MALE; MEMORY, SHORT-TERM; MOLECULAR TARGETED THERAPY; NEURONS; POLYUNSATURATED ALKAMIDES; RATS; RATS, LONG-EVANS;

EID: 80051799610     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2011.07.003     Document Type: Article

References (70)

1. H. Abush, and I. Akirav Cannabinoids modulate hippocampal memory and plasticity Hippocampus 20 2010 1126 1138
2. D.M. Barros, V. Carlis, M. Maidana, E.S. Silva, A.L. Baisch, M.R. Ramirez, and I. Izquierdo Interactions between anandamide-induced anterograde amnesia and post-training memory modulatory systems Brain Res. 1016 2004 66 71 (Pubitemid 38842453)
3. M.D. Bhaskaran, and B.N. Smith Effects of TRPV1 activation on synaptic excitation in the dentate gyrus of a mouse model of temporal lobe epilepsy Exp. Neurol. 223 2010 529 536
4. R.M. Bitencourt, F.A. Pamplona, and R.N. Takahashi Facilitation of contextual fear memory extinction and anti-anxiogenic effects of AM404 and cannabidiol in conditioned rats Eur. Neuropsychopharmacol. 18 2008 849 859
5. J. Breyne, and B. Vanheel Methanandamide hyperpolarizes gastric arteries by stimulation of TRPV1 receptors on perivascular CGRP containing nerves J. Cardiovasc. Pharmacol. 47 2006 303 309 (Pubitemid 44384070)
6. J. Brodkin, and J.M. Moerschbaecher SR141716A antagonizes the disruptive effects of cannabinoid ligands on learning in rats J. Pharmacol. Exp. Ther. 282 1997 1526 1532 (Pubitemid 27408337)
7. C. Castellano, S. Cabib, A. Palmisano, V. DiMarzo, and S. Puglisi-Allegra The effects of anandamide on memory consolidation in mice involve both D1 and D2 dopamine receptors Behav. Pharmacol. 8 1997 707 712 (Pubitemid 28040002)
8. C. Castellano, R. Ventura, S. Cabib, and S. Puglisi-Allegra Strain-dependent effects of anandamide on memory consolidation in mice are antagonized by naltrexone Behav. Pharmacol. 10 1999 453 457 (Pubitemid 29440553)
9. A.E. Chavez, C.Q. Chiu, and P.E. Castillo TRPV1 activation by endogenous anandamide triggers postsynaptic long-term depression in dentate gyrus Nat. Neurosci. 13 2010 1511 1518
10. J.P. Chhatwal, M. Davis, K.A. Maguschak, and K.J. Ressler Enhancing cannabinoid neurotransmission augments the extinction of conditioned fear Neuropsychopharmacology 30 2005 516 524 (Pubitemid 40271154)
11. B. Coomber, M.F. O'Donoghue, and R. Mason Inhibition of endocannabinoid metabolism attenuates enhanced hippocampal neuronal activity induced by kainic acid Synapse 62 2008 746 755
12. M. Costanzi, M. Battaglia, R. Populin, V. Cestari, and C. Castellano Anandamide and memory in CD1 mice: effects of immobilization stress and of prior experience Neurobiol. Learn. Mem. 79 2003 204 211 (Pubitemid 36382916)
13. S.A. Deadwyler, T. Bunn, and R.E. Hampson Hippocampal ensemble activity during spatial delayed-nonmatch-to-sample performance in rats J. Neurosci. 16 1996 354 372 (Pubitemid 26010722)
14. S.A. Deadwyler, A.V. Goonawardena, and R.E. Hampson Short-term memory is modulated by the spontaneous release of endocannabinoids: evidence from hippocampal population codes Behav. Pharmacol. 18 2007 571 580 (Pubitemid 47356383)
15. S.A. Deadwyler, and R.E. Hampson Differential but complementary mnemonic functions of the hippocampus and subiculum Neuron 42 2004 465 476 (Pubitemid 38610144)
16. W.A. Devane, L. Hanus, A. Breuer, R.G. Pertwee, L.A. Stevenson, G. Griffin, D. Gibson, A. Mandelbaum, A. Etinger, and R. Mechoulam Isolation and structure of a brain constituent that binds to the cannabinoid receptor Science 258 1992 1946 1949 (Pubitemid 23026736)
17. V. Di Marzo, S.K. Goparaju, L. Wang, J. Liu, S. Batkai, Z. Jarai, F. Fezza, G.I. Miura, R.D. Palmiter, T. Sugiura, and G. Kunos Leptin-regulated endocannabinoids are involved in maintaining food intake Nature 410 2001 822 825 (Pubitemid 32303781)
18. M.R. Domenici, S.C. Azad, G. Marsicano, A. Schierloh, C.T. Wotjak, H.U. Dodt, W. Zieglgansberger, B. Lutz, and G. Rammes Cannabinoid receptor type 1 located on presynaptic terminals of principal neurons in the forebrain controls glutamatergic synaptic transmission J. Neurosci. 26 2006 5794 5799 (Pubitemid 44315272)
19. D. Fegley, S. Kathuria, R. Mercier, C. Li, A. Goutopoulos, A. Makriyannis, and D. Piomelli Anandamide transport is independent of fatty-acid amide hydrolase activity and is blocked by the hydrolysis-resistant inhibitor AM1172 Proc. Natl. Acad. Sci. U.S.A. 101 2004 8756 8761 (Pubitemid 38745844)
20. F. Ferrari, A. Ottani, R. Vivoli, and D. Giuliani Learning impairment produced in rats by the cannabinoid agonist HU 210 in a water-maze task Pharmacol. Biochem. Behav. 64 1999 555 561 (Pubitemid 29488485)
21. C.J. Fowler, G. Tiger, A. Ligresti, M.L. Lopez-Rodriguez, and V. Di Marzo Selective inhibition of anandamide cellular uptake versus enzymatic hydrolysis-a difficult issue to handle Eur. J. Pharmacol. 492 2004 1 11 (Pubitemid 38624415)
22. T.F. Freund, I. Katona, and D. Piomelli Role of endogenous cannabinoids in synaptic signaling Physiol. Rev. 83 2003 1017 1066 (Pubitemid 36828930)
23. S.T. Glaser, N.A. Abumrad, F. Fatade, M. Kaczocha, K.M. Studholme, and D.G. Deutsch Evidence against the presence of an anandamide transporter Proc. Natl. Acad. Sci. U.S.A. 100 2003 4269 4274 (Pubitemid 36418192)
24. S.T. Glaser, D.G. Deutsch, K.M. Studholme, S. Zimov, and S. Yazulla Endocannabinoids in the intact retina: 3 H-anandamide uptake, fatty acid amide hydrolase immunoreactivity and hydrolysis of anandamide Vis. Neurosci. 22 2005 693 705 (Pubitemid 43237733)
25. A.V. Goonawardena, L. Robinson, R.E. Hampson, and G. Riedel Cannabinoid and cholinergic systems interact during performance of a short-term memory task in the rat Learn. Mem. 17 2010 502 511
26. A.V. Goonawardena, L. Robinson, G. Riedel, and R.E. Hampson Recruitment of hippocampal neurons to encode behavioral events in the rat: alterations in cognitive demand and cannabinoid exposure Hippocampus 20 2010 1083 1094
27. R.E. Hampson, and S.A. Deadwyler Cannabinoids, hippocampal function and memory Life Sci. 65 1999 715 723 (Pubitemid 29362777)
28. R.E. Hampson, and S.A. Deadwyler Cannabinoids reveal the necessity of hippocampal neural encoding for short-term memory in rats J. Neurosci. 20 2000 8932 8942
29. R.E. Hampson, J.D. Simeral, E.J. Kelly, and S.A. Deadwyler Tolerance to the memory disruptive effects of cannabinoids involves adaptation by hippocampal neurons Hippocampus 13 2003 543 556 (Pubitemid 36958279)
30. H.S. Hansen Palmitoylethanolamide and other anandamide congeners. Proposed role in the diseased brain Exp. Neurol. 224 2010 48 55
31. M. Herkenham, A.B. Lynn, M.R. Johnson, L.S. Melvin, B.R. De Costa, and K.C. Rice Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study J. Neurosci. 11 1991 563 583
32. C.J. Heyser, R.E. Hampson, and S.A. Deadwyler 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 1993 294 307 (Pubitemid 23309216)
33. C.J. Hillard, W.S. Ho, J. Thompson, K.M. Gauthier, C.E. Wheelock, H. Huang, and B.D. Hammock Inhibition of 2-arachidonoylglycerol catabolism modulates vasoconstriction of rat middle cerebral artery by the thromboxane mimetic, U-46619 Br. J. Pharmacol. 152 2007 691 698 (Pubitemid 350034988)
34. C.J. Hillard, and A. Jarrahian The movement of N-arachidonoylethanolamine (anandamide) across cellular membranes Chem. Phys. Lipids 108 2000 123 134
35. W.S. Ho, D.A. Barrett, and M.D. Randall 'Entourage' effects of N-palmitoylethanolamide and N-oleoylethanolamide on vasorelaxation to anandamide occur through TRPV1 receptors Br. J. Pharmacol. 155 2008 837 846
36. B.G. Kelley, and S.A. Thayer Anandamide transport inhibitor AM404 and structurally related compounds inhibit synaptic transmission between rat hippocampal neurons in culture independent of cannabinoid CB1 receptors Eur. J. Pharmacol. 496 2004 33 39 (Pubitemid 39024313)
37. D. Kim, and S.A. Thayer Cannabinoids inhibit the formation of new synapses between hippocampal neurons in culture J. Neurosci. 21 2001 RC146
38. A.R. King, A. Duranti, A. Tontini, S. Rivara, A. Rosengarth, J.R. Clapper, G. Astarita, J.A. Geaga, H. Luecke, M. Mor, G. Tarzia, and D. Piomelli URB602 inhibits monoacylglycerol lipase and selectively blocks 2-arachidonoylglycerol degradation in intact brain slices Chem. Biol. 14 2007 1357 1365 (Pubitemid 350257009)
39. P. Kosiorek, A. Hryniewicz, I. Bialuk, A. Zawadzka, and M.M. Winnicka Cannabinoids alter recognition memory in rats Pol. J. Pharmacol. 55 2003 903 910 (Pubitemid 37540888)
40. G. Lees, and A. Dougalis Differential effects of the sleep-inducing lipid oleamide and cannabinoids on the induction of long-term potentiation in the CA1 neurons of the rat hippocampus in vitro Brain Res. 997 2004 1 14 (Pubitemid 38058529)
41. A.H. Lichtman SR 141716A enhances spatial memory as assessed in a radial-arm maze task in rats Eur. J. Pharmacol. 404 2000 175 179
42. A.H. Lichtman, K.R. Dimen, and B.R. Martin Systemic or intrahippocampal cannabinoid administration impairs spatial memory in rats Psychopharmacology (Berl) 119 1995 282 290
43. A. Ligresti, E. Morera, M. van der Stelt, K. Monory, B. Lutz, G. Ortar, and V. Di Marzo Further evidence for the existence of a specific process for the membrane transport of anandamide Biochem. J. 380 2004 265 272 (Pubitemid 38725751)
44. J.Z. Long, W. Li, L. Booker, J.J. Burston, S.G. Kinsey, J.E. Schlosburg, F.J. Pavón, A.M. Serrano, D.E. Selley, L.H. Parsons, A.H. Lichtman, and B.F. Cravatt Selective blockade of 2-arachidonoylglycerol hydrolysis produces cannabinoid behavioral effects Nat. Chem. Biol. 5 2009 37 44
45. P.E. Mallet, and R.J. Beninger The cannabinoid CB1 receptor antagonist SR141716A attenuates the memory impairment produced by delta9- tetrahydrocannabinol or anandamide Psychopharmacology (Berl) 140 1998 11 19 (Pubitemid 28524302)
46. G. Marsicano, and B. Lutz Expression of the cannabinoid receptor CB1 in distinct Neuronal subpopulations in the adult mouse forebrain Eur. J. Neurosci. 11 1999 4213 4225 (Pubitemid 30009252)
47. G. Marsicano, C.T. Wotjak, S.C. Azad, T. Bisogno, G. Rammes, and M.G. Cascio The endogenous cannabinoid system controls extinction of aversive memories Nature 418 2002 530 534 (Pubitemid 34851398)
48. C. Mazzola, J. Medalie, M. Scherma, L.V. Panlilio, M. Solinas, G. Tanda, F. Drago, J.L. Cadet, S.R. Goldberg, and S. Yasar Fatty acid amide hydrolase (FAAH) inhibition enhances memory acquisition through activation of PPAR-alpha nuclear receptors Learn. Mem. 16 2009 332 337
49. C. Mazzola, V. Micale, and F. Drago Amnesia induced by beta-amyloid fragments is counteracted by cannabinoid CB1 receptor blockade Eur. J. Pharmacol. 477 2003 219 225 (Pubitemid 38366394)
50. K. Mishima, N. Egashira, N. Hirosawa, M. Fujii, Y. Matsumoto, K. Iwasaki, and M. Fujiwara Characteristics of learning and memory impairment induced by delta 9-tetrahydrocannabinol in rats Jpn. J. Pharmacol. 87 2001 297 308
51. E. Murillo-Rodriguez, M. Sanchez-Alavez, L. Navarro, D. Martinez-Gonzalez, R. Drucker-Colin, and O. Prospero-Garcia Anandamide modulates sleep and memory in rats Brain Res. 812 1998 270 274 (Pubitemid 29005359)
52. Y. Ning, K. O'Neill, H. Lan, L. Pang, L.X. Shan, B.E. Hawes, and J.A. Hedrick Endogenous and synthetic agonists of GPR119 differ in signalling pathways and their effects on insulin secretion in MIN6c4 insulinoma cells Br. J. Pharmacol. 155 2008 1056 1065
53. F.A. Pamplona, R.M. Bitencourt, and R.N. Takahashi Short- and long-term effects of cannabinoids on the extinction of contextual fear memory in rats Neurobiol. Learn. Mem. 90 2008 290 293
54. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates fourth ed. 1998 Academic Press New York
55. G. Pillolla, M. Melis, S. Perra, A.L. Muntoni, G.L. Gessa, and M. Pistis Medial forebrain bundle stimulation evokes endocannabinoid-mediated modulation of ventral tegmental area dopamine neuron firing in vivo Psychopharmacology (Berl) 191 2007 843 853 (Pubitemid 46355909)
56. L.A. Roberts, H.R. Ross, and M. Connor Methanandamide activation of a novel current in mouse trigeminal ganglion sensory neurons in vitro Neuropharmacology 54 1 2008 172 180 (Pubitemid 350299396)
57. L. Robinson, A.V. Goonawardena, R. Pertwee, R.E. Hampson, B. Platt, and G. Riedel WIN55,212-2 induced deficits in spatial learning are mediated by cholinergic hypofunction Behav. Brain Res. 208 2010 584 592
58. L. Robinson, S. McKillop-Smith, N.L. Ross, R.G. Pertwee, R.E. Hampson, B. Platt, and G. Riedel Hippocampal endocannabinoids inhibit spatial learning and limit spatial memory in rats Psychopharmacology (Berl) 198 2008 551 563
59. J. Ronesi, G.L. Gerdeman, and D.M. Lovinger Disruption of endocannabinoid release and striatal long-term depression by postsynaptic blockade of endocannabinoid membrane transport J. Neurosci. 24 2004 1673 1679 (Pubitemid 38240964)
60. A. Seillier, T. Advani, T. Cassano, J.G. Hensler, and A. Giuffrida Inhibition of fatty-acid amide hydrolase and CB1 receptor antagonism differentially affect behavioural responses in normal and PCP-treated rats Int. J. Neuropsychopharmacol. 13 2010 373 386
61. N. Stella, P. Schweitzer, and D. Piomelli A second endogenous cannabinoid that modulates long-term potentiation Nature 388 1997 773 778 (Pubitemid 27375156)
62. A. Suzuki, S.A. Josselyn, P.W. Frankland, S. Masushige, A.J. Silva, and S. Kida Memory reconsolidation and extinction have distinct temporal and biochemical signatures J. Neurosci. 24 2004 4787 4795 (Pubitemid 38668203)
63. J.P. Terranova, J.C. Michaud, G. Le Fur, and P. Soubrie 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 1995 576 579
64. J.P. Terranova, J.J. Storme, N. Lafon, A. Perio, M. Rinaldi-Carmona, and G. Le Fur Improvement of memory in rodents by the selective CB1 cannabinoid receptor antagonist, SR 141716 Psychopharmacology (Berl) 126 1996 165 172 (Pubitemid 26246767)
65. A. Toth, J. Boczan, N. Kedei, E. Lizanecz, Z. Bagi, Z. Papp, I. Edes, L. Csiba, and P.M. Blumberg Expression and distribution of vanilloid receptor 1 (TRPV1) in the adult rat brain Brain Res. Mol. Brain Res. 135 2005 162 168 (Pubitemid 40602409)
66. S.A. Varvel, and A.H. Lichtman Evaluation of CB1 receptor knockout mice in the Morris water maze J. Pharmacol. Exp. Ther. 301 2002 915 924 (Pubitemid 34595080)
67. S.A. Varvel, E.A. Anum, and A.H. Lichtman Disruption of CB(1) receptor signaling impairs extinction of spatial memory in mice Psychopharmacology (Berl) 179 2005 863 872 (Pubitemid 40767906)
68. S.A. Varvel, B.F. Cravatt, A.E. Engram, and A.H. Lichtman Fatty acid amide hydrolase (-/-) mice exhibit an increased sensitivity to the disruptive effects of anandamide or oleamide in a working memory water maze task J. Pharmacol. Exp. Ther. 317 2006 251 257
69. L.E. Wise, R. Cannavacciulo, B.F. Cravatt, B.F. Martin, and A.H. Lichtman Evaluation of fatty acid amides in the carrageenan-induced paw edema model Neuropharmacology 54 2008 181 188 (Pubitemid 350299403)
70. M.C. Wolff, and J.D. Leander SR141716A, a cannabinoid CB1 receptor antagonist, improves memory in a delayed radial maze task Eur. J. Pharmacol. 477 2003 213 217 (Pubitemid 38366393)