A primary cortical input to hippocampus expresses a pathway-specific and endocannabinoid-dependent form of long-term potentiation

eNeuro

Volumn 3, Issue 4, 2016, Pages 10049-10053

  Wang, Weisheng ^a   Trieu, Brian H ^a   Palmer, Linda C ^a   Jia, Yousheng ^a   Pham, Danielle T ^a   Jung, Kwang Mook ^a   Karsten, Carley A ^a   Merrill, Collin B ^a   Mackie, Ken ^b   Gall, Christine M ^a   Piomelli, Daniele ^a,c,d   Lynch, Gary ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INDIANA UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; CANNABINOID RECEPTOR; ENDOCANNABINOID; GLUTAMATE RECEPTOR; LATRUNCULIN A; ACTIN; ACYLGLYCEROL LIPASE; CANNABINOID 1 RECEPTOR;

ACTIN POLYMERIZATION; ADRENAL CORTEX; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLUMN CHROMATOGRAPHY; CONTROLLED STUDY; DENTATE GYRUS; DEPRESSION; ELECTROPHYSIOLOGY; ENTORHINAL CORTEX; EVOKED RESPONSE; GENE OVEREXPRESSION; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL SLICE; HIPPOCAMPUS; IMMUNOFLUORESCENCE TEST; LIQUID CHROMATOGRAPHY; LONG TERM POTENTIATION; MALE; MASS SPECTROMETRY; MOUSE; NEUROTRANSMITTER RELEASE; NONHUMAN; OLFACTORY DISCRIMINATION; PERFORANT NERVE TRACT; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; RAT; SCHAFFER COLLATERAL PATHWAY; SIGNAL TRANSDUCTION; STIMULATION; SYNAPTIC TRANSMISSION; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN CORTEX; CYTOLOGY; DRUG EFFECTS; EXCITATORY POSTSYNAPTIC POTENTIAL; GENETICS; LONG EVANS RAT; METABOLISM; NERVE ENDING; NERVE TRACT; PERCEPTIVE DISCRIMINATION; PHYSIOLOGY; SMELLING; SPRAGUE DAWLEY RAT; TISSUE CULTURE TECHNIQUE; TRANSGENIC MOUSE;

ACTINS; ANIMALS; CEREBRAL CORTEX; DISCRIMINATION (PSYCHOLOGY); ENDOCANNABINOIDS; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; MICE, TRANSGENIC; MONOACYLGLYCEROL LIPASES; NEURAL PATHWAYS; OLFACTORY PERCEPTION; PRESYNAPTIC TERMINALS; RATS, LONG-EVANS; RATS, SPRAGUE-DAWLEY; RECEPTOR, CANNABINOID, CB1; TISSUE CULTURE TECHNIQUES;

EID: 85019547240     PISSN: None     EISSN: 23732822     Source Type: Journal    
DOI: 10.1523/ENEURO.0160-16.2016     Document Type: Article

References (114)

1. Abraham WC, Christie BR, Logan B, Lawlor P, Dragunow M (1994) Immediate early gene expression associated with the persistence of heterosynaptic long-term depression in the hippocampus. Proc Natl Acad Sci U S A 91: 10049-10053. Medline
2. Amaral D, Lavenex P (2007) Hippocampal neuroanatomy. In: The hippocampus book (Andersen P, Morris RG, Amaral D, Bliss TV, O’Keefe J, eds), pp 37-114. New York: Oxford UP.
3. Atsak P, Hauer D, Campolongo P, Schelling G, Fornari RV, Roozendaal B (2015) Endocannabinoid signaling integrates multiple stress hormone effects on memory consolidation. Psychoneuroendocrinology 61: 5. CrossRef Medline
4. Babayan AH, Kramár EA, Barrett RM, Jafari M, Häettig J, Chen LY, Rex CS, Lauterborn JC, Wood MA, Gall CM, Lynch G (2012) Integrin dynamics produce a delayed stage of long-term potenti- ation and memory consolidation. J Neurosci 32: 12854-12861. CrossRef Medline
5. Bisogno T, Howell F, Williams G, Minassi A, Cascio MG, Ligresti A, Matias I, Schiano-Moriello A, Paul P, Williams EJ, Gangadharan U, Hobbs C, Di Marzo V, Doherty P (2003) Cloning of the first sn1-DAG lipases points to the spatial and temporal regulation of endocannabinoid signaling in the brain. J Cell Biol 163: 463-468. CrossRef
6. 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. Medline
7. Bozdagi O, Wang XB, Nikitczuk JS, Anderson TR, Bloss EB, Radice GL, Zhou Q, Benson DL, Huntley GW (2010) Persistence of coordinated long-term potentiation and dendritic spine enlargement at mature hippocampal CA1 synapses requires N-cadherin. J Neurosci 30: 9984-9989. CrossRef Medline
8. Bramham CR (2008) Local protein synthesis, actin dynamics, and LTP consolidation. Curr Opin Neurobiol 18: 524-531. CrossRef Medline
9. Bramham CR, Errington ML, Bliss TV (1988) Naloxone blocks the induction of long-term potentiation in the lateral but not in the medial perforant pathway in the anesthetized rat. Brain Res 449: 352-356. Medline
10. Burwell RD (2000) The parahippocampal region: corticocortical connectivity. Ann N Y Acad Sci 911: 25-42. Medline
11. Carlson G, Wang Y, Alger BE (2002) Endocannabinoids facilitate the induction of LTP in the hippocampus. Nat Neurosci 5: 723-724. CrossRef Medline
12. Castillo PE, Younts TJ, Chávez AE, Hashimotodani Y (2012) Endocannabinoid signaling and synaptic function. Neuron 76: 70-81. CrossRef Medline
13. Chen LY, Rex CS, Sanaiha Y, Lynch G, Gall CM (2010) Learning induces neurotrophin signaling at hippocampal synapses. Proc Natl Acad Sci U S A 107: 7030-7035. CrossRef Medline
14. Chiu CQ, Castillo PE (2008) Input-specific plasticity at excitatory synapses mediated by endocannabinoids in the dentate gyrus. Neuropharmacology 54: 68-78. CrossRef Medline
15. Christie BR, Abraham WC (1994) Differential regulation of pairedpulse plasticity following LTP in the dentate gyrus. Neuroreport 5: 385-388. Medline
16. Colgin LL, Kramár EA, Gall CM, Lynch G (2003) Septal modulation of excitatory transmission in hippocampus. J Neurophysiol 90: 2358-2366. CrossRef Medline
17. Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, Moser MB, Moser EI (2009) Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 462: 353-357. CrossRef Medline
18. Cui Y, Paillé V, Xu H, Genet S, Delord B, Fino E, Berry H, Venance L (2015) Endocannabinoids mediate bidirectional striatal spiketiming- dependent plasticity. J Physiol 593: 2833-2849. CrossRef Medline
19. Dalton GD, Peterson LJ, Howlett AC (2013) CB1 cannabinoid receptors promote maximal FAK catalytic activity by stimulating cooperative signaling between receptor tyrosine kinases and integrins in neuronal cells. Cell Signal 25: 1665-1677. CrossRef Medline
20. Dani A, Huang B, Bergan J, Dulac C, Zhuang X (2010) Superresolution imaging of chemical synapses in the brain. Neuron 68: 843-856. CrossRef Medline
21. Deng L, Cornett BL, Mackie K, Hohmann AG (2015) CB1 knockout mice unveil sustained CB2-mediated antiallodynic effects of the mixed CB1/CB2 agonist CP55,940 in a mouse model of paclitaxelinduced neuropathic pain. Mol Pharmacol 88: 64-74. CrossRef
22. Derkinderen P, Toutant M, Kadaré G, Ledent C, Parmentier M, Girault JA (2001) Dual role of Fyn in the regulation of FAK+6,7 by cannabinoids in hippocampus. J Biol Chem 276: 38289-38296. CrossRef Medline
23. Do VH, Martinez CO, Martinez JL Jr, Derrick BE (2002) Long-term potentiation in direct perforant path projections to the hippocampal CA3 region in vivo. J Neurophysiol 87: 669-678.
24. Dunwiddie T, Lynch G (1978) Long-term potentiation and depression of synaptic responses in the rat hippocampus: localization and frequency dependency. J Physiol 276: 353-367. Medline
25. Eichenbaum H (2014) Time cells in the hippocampus: a new dimension for mapping memories. Nat Rev Neurosci 15: 732-744. Cross-Ref Medline
26. Fedulov V, Rex CS, Simmons DA, Palmer L, Gall CM, Lynch G (2007) Evidence that long-term potentiation occurs within individual hippocampal synapses during learning. J Neurosci 27: 8031-8039. CrossRef Medline
27. Gómez-Gonzalo M, Navarrete M, Perea G, Covelo A, Martín-Fernández M, Shigemoto R, Luján R, Araque A (2015) Endocannabinoids induce lateral long-term potentiation of transmitter release by stimulation of gliotransmission. Cereb Cortex 25: 3699-3712. CrossRef Medline
28. Goodman J, Packard MG (2015) The influence of cannabinoids on learning and memory processes of the dorsal striatum. Neurobiol Learn Mem 125: 1-14. CrossRef Medline
29. Granger AJ, Nicoll RA (2014) Expression mechanisms underlying long-term potentiation: a postsynaptic view, 10 years on. Philos Trans R Soc Lond B Biol Sci 369: 20130136 CrossRef Medline
30. Gulyas AI, Cravatt BF, Bracey MH, Dinh TP, Piomelli D, Boscia F, Freund TF (2004) Segregation of two endocannabinoidhydrolyzing enzymes into pre- and postsynaptic compartments in the rat hippocampus, cerebellum and amygdala. Eur J Neurosci 20: 441-458. CrossRef Medline
31. Hampson RE, Sweatt AJ, Goonawardena AV, Song D, Chan RH, Marmarelis VZ, Berger TW, Deadwyler SA (2011) Memory encoding in hippocampal ensembles is negatively influenced by cannabinoid CB1 receptors. Behav Pharmacol 22: 335-346. CrossRef Medline
32. Hanse E, Gustafsson B (1992) Postsynaptic, but not presynaptic, activity controls the early time course of long-term potentiation in the dentate gyrus. J Neurosci 12: 3226-3240.
33. Harney SC, Jane DE, Anwyl R (2008) Extrasynaptic NR2D-containing NMDARs are recruited to the synapse during LTP of NMDAREPSCs. J Neurosci 28: 11685-11694. CrossRef Medline
34. He JC, Gomes I, Nguyen T, Jayaram G, Ram PT, Devi LA, Iyengar R (2005) The G alpha(o/i)-coupled cannabinoid receptor-mediated neurite outgrowth involves Rap regulation of Src and Stat3. J Biol Chem 280: 33426-33434. CrossRef
35. Hofmann ME, Nahir B, Frazier CJ (2008) Excitatory afferents to CA3 pyramidal cells display differential sensitivity to CB1 dependent inhibition of synaptic transmission. Neuropharmacology 55: 1140-1146. CrossRef Medline
36. Howlett AC, Mukhopadhyay S (2000) Cellular signal transduction by anandamide and 2-arachidonoylglycerol. Chem Phys Lipids 108: 53-70. Medline
37. Insausti R, Amaral DG, Cowan WM (1987) The entorhinal cortex of the monkey: II. Cortical afferents. J Comp Neur 264: 356-395. CrossRef Medline
38. Iversen LL (2008) The science of marijuana. New York: Oxford UP.
39. Jia Y, Gall CM, Lynch G (2010) Presynaptic BDNF promotes postsynaptic long-term potentiation in the dorsal striatum. J Neurosci 30: 14440-14445. CrossRef Medline
40. Jung KM, Mangieri R, Stapleton C, Kim J, Fegley D, Wallace M, Mackie K, Piomelli D (2005) Stimulation of endocannabinoid formation in brain slice cultures through activation of group I metabotropic glutamate receptors. Mol Pharmacol 68: 1196-1202. CrossRef
41. Jung KM, Astarita G, Zhu C, Wallace M, Mackie K, Piomelli D (2007) A key role for diacylglycerol lipase-alpha in metabotropic glutamate receptor-dependent endocannabinoid mobilization. Mol Pharmacol 72: 612-621. CrossRef Medline
42. Jung KM, Sepers M, Henstridge CM, Lassalle O, Neuhofer D, Martin H, Ginger M, Frick A, DiPatrizio NV, Mackie K, Katona I, Piomelli D, Manzoni OJ (2012a) Uncoupling of the endocannabinoid signalling complex in a mouse model of fragile X syndrome. Nat Commun 3: 1080 CrossRef Medline
43. Jung KM, Clapper JR, Fu J, D’Agostino G, Guijarro A, Thongkham D, Avanesian A, Astarita G, DiPatrizio NV, Frontini A, Cinti S, Diano S, Piomelli D (2012b) 2-Arachidonoylglycerol signaling in forebrain regulates systemic energy metabolism. Cell Metab 15: 299-310. CrossRef Medline
44. Kano M, Ohno-Shosaku T, Hashimotodani Y, Uchigashima M, Watanabe M (2009) Endocannabinoid-mediated control of synaptic transmission. Physiol Rev 89: 309-380. CrossRef Medline
45. Katona I, Urbán GM, Wallace M, Ledent C, Jung KM, Piomelli D, Mackie K, Freund TF (2006) Molecular composition of the endocannabinoid system at glutamatergic synapses. J Neurosci 26: 5628-5637. CrossRef Medline
46. Kauer JA, Malenka RC, Nicoll RA (1988) A persistent postsynaptic modification mediates long-term potentiation in the hippocampus. Neuron 1: 911-917. Medline
47. Keimpema E, Mackie K, Harkany T (2011) Molecular model of cannabis sensitivity in developing neuronal circuits. Trends Pharmacol Sci 32: 551-561. CrossRef Medline
48. Kerchner GA, Nicoll RA (2008) Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nat Rev Neurosci 9: 813-825. CrossRef Medline
49. Khaspekov LG, Brenz Verca MS, Frumkina LE, Hermann H, Marsicano G, Lutz B (2004) Involvement of brain-derived neurotrophic factor in cannabinoid receptor-dependent protection against excitotoxicity. Eur J Neurosci 19: 1691-1698. CrossRef
50. 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.
51. King AR, Duranti A, Tontini A, Rivara S, Rosengarth A, Clapper JR, Astarita G, Geaga JA, Luecke H, Mor M, Tarzia G, Piomelli D (2007) URB602 inhibits monoacylglycerol lipase and selectively blocks 2-arachidonoylglycerol degradation in intact brain slices. Chem Biol 14: 1357-1365. CrossRef Medline
52. Korte M, Kang H, Bonhoeffer T, Schuman E (1998) A role for BDNF in the late-phase of hippocampal long-term potentiation. Neuropharmacology 37: 553-559. Medline
53. Kramár EA, Lin B, Rex CS, Gall CM, Lynch G (2006) Integrin-driven actin polymerization consolidates long-term potentiation. Proc Natl Acad Sci U S A 103: 5579-5584. CrossRef Medline
54. Kramár EA, Chen LY, Brandon NJ, Rex CS, Liu F, Gall CM, Lynch G (2009) Cytoskeletal changes underlie estrogen’s acute effects on synaptic transmission and plasticity. J Neurosci 29: 12982-12993. CrossRef Medline
55. Kramár EA, Babayan AH, Gavin CF, Cox CD, Jafari M, Gall CM, Rumbaugh G, Lynch G (2012) Synaptic evidence for the efficacy of spaced learning. Proc Natl Acad Sci U S A 109: 5121-5126. Cross-Ref Medline
56. Lam PY, Mangos S, Green JM, Reiser J, Huttenlocher A (2015) In vivo imaging and characterization of actin microridges. PLoS One 10: e0115639. CrossRef Medline
57. Larson J, Lynch G (1989) Theta pattern stimulation and the induction of LTP: the sequence in which synapses are stimulated determines the degree to which they potentiate. Brain Res 489: 49-58. Medline
58. Larson J, Wong D, Lynch G (1986) Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Res 368: 347-350. Medline
59. Larson J, Lieu T, Petchpradub V, LeDuc B, Ngo H, Rogers GA, Lynch G (1995) Facilitation of olfactory learning by a modulator of AMPA receptors. J Neurosci 15: 8023-8030. Medline
60. Lin B, Colgin LL, Brücher FA, Arai AC, Lynch G (2002) Interactions between recording technique and AMPA receptor modulators. Brain Res 955: 164-173. Medline
61. Lin QS, Yang Q, Liu DD, Sun Z, Dang H, Liang J, Wang YX, Chen J, Li ST (2011) Hippocampal endocannabinoids play an important role in induction of long-term potentiation and regulation of contextual fear memory formation. Brain Res Bull 86: 139-145. Cross-Ref Medline
62. Long JZ, Nomura DK, Cravatt BF (2009) Characterization of monoacylglycerol lipase inhibition reveals differences in central and peripheral endocannabinoid metabolism. Chem Biol 16: 744-753. CrossRef Medline
63. Lovinger DM, Routtenberg A (1988) Synapse-specific protein kinase C activation enhances maintenance of long-term potentiation in rat hippocampus. J Physiol 400: 321-333. Medline
64. Lynch G, Gall CM (2013) Mechanism based approaches for rescuing and enhancing cognition. Front Neurosci 7: 143. CrossRef Medline
65. Lynch G, Kramár EA, Babayan AH, Rumbaugh G, Gall CM (2013) Differences between synaptic plasticity thresholds result in new timing rules for maximizing long-term potentiation. Neuropharmacology 64: 27-36. CrossRef Medline
66. Mackie K (2008) Cannabinoid receptors: where they are and what they do. J Neuroendocrinol 20 [Suppl 1]: 10-14. CrossRef Medline
67. Mai P, Tian L, Yang L, Wang L, Yang L, Li L (2015) Cannabinoid receptor 1 but not 2 mediates macrophage phagocytosis by G(α)i/o/RhoA/ROCK signaling pathway. J Cell Physiol 230: 1640-1650. CrossRef Medline
68. Malenczyk K, Jazurek M, Keimpema E, Silvestri C, Janikiewicz J, Mackie K, Di Marzo V, Redowicz MJ, Harkany T, Dobrzyn A (2013) CB1 cannabinoid receptors couple to focal adhesion kinase to control insulin release. J Biol Chem 288: 32685-32699. CrossRef Medline
69. Manabe T, Nicoll RA (1994) Long-term potentiation: evidence against an increase in transmitter release probability in the CA1 region of the hippocampus. Science 265: 1888-1892. Medline
70. Martens KM, Vonder Haar C, Hutsell BA, Hoane MR (2013) The dig task: a simple scent discrimination reveals deficits following frontal brain damage. J Vis Exp e50033.
71. Mátyás F, Yanoversusky Y, Mackie K, Kelsch W, Misgeld U, Freund TF (2006) Subcellular localization of type 1 cannabinoid receptors in the rat basal ganglia. Neuroscience 137: 337-361. CrossRef Medline
72. Mátyás F, Watanabe M, Mackie K, Katona I, Freund TF (2007) Molecular architecture of the cannabinoid signaling system in the core of the nucleus accumbens. Ideggyogy Sz 60: 187-191. Medline
73. Mody I, Salter MW, MacDonald JF (1988) Requirement of NMDA receptor/channels for intracellular high-energy phosphates and the extent of intraneuronal calcium buffering in cultured mouse hippocampal neurons. Neurosci Lett 93: 73-78. Medline
74. Moreno-Sanz G, Duranti A, Melzig L, Fiorelli C, Ruda GF, Colombano G, Mestichelli P, Sanchini S, Tontini A, Mor M, Bandiera T, Scarpelli R, Tarzia G, Piomelli D (2013) Synthesis and structure-activity relationship studies of O-biphenyl-3-yl carbamates as peripherally restricted fatty acid amide hydrolase inhibitors. J Med Chem 56: 5917-5930. CrossRef Medline
75. Morris RG (2003) Long-term potentiation and memory. Philos Trans R Soc Lond B Biol Sci 358: 643-647. CrossRef Medline
76. Muller D, Lynch G (1988) Long-term potentiation differentially affects two components of synaptic responses in hippocampus. Proc Natl Acad Sci U S A 85: 9346-9350. Medline
77. Nabavi S, Fox R, Proulx CD, Lin JY, Tsien RY, Malinow R (2014) Engineering a memory with LTD and LTP. Nature 511: 348-352. CrossRef Medline
78. Navarrete M, Araque A (2010) Endocannabinoids potentiate synaptic transmission through stimulation of astrocytes. Neuron 68: 113-126. CrossRef Medline
79. Naydenov AV, Horne EA, Cheah CS, Swinney K, Hsu KL, Cao JK, Marrs WR, Blankman JL, Tu S, Cherry AE, Fung S, Wen A, Li W, Saporito MS, Selley DE, Cravatt BF, Oakley JC, Stella N (2014) ABHD6 blockade exerts antiepileptic activity in PTZ-induced seizures and in spontaneous seizures in R6/2 mice. Neuron 83: 361-371. CrossRef Medline
80. Nicoll RA, Schmitz D (2005) Synaptic plasticity at hippocampal mossy fibre synapses. Nat Rev Neurosci 6: 863-876. CrossRef Medline
81. Nithipatikom K, Gomez-Granados AD, Tang AT, Pfeiffer AW, Williams CL, Campbell WB (2012) Cannabinoid receptor type 1 (CB1) activation inhibits small GTPase RhoA activity and regulates mo- tility of prostate carcinoma cells. Endocrinology 153: 29-41. CrossRef Medline
82. Njoo C, Agarwal N, Lutz B, Kuner R (2015) The cannabinoid receptor CB1 interacts with the WAVE1 complex and plays a role in actin dynamics and structural plasticity in neurons. PLoS Biol 13: e1002286. CrossRef Medline
83. Otto T, Schottler F, Staubli U, Eichenbaum H, Lynch G (1991) Hippocampus and olfactory discrimination learning: effects of entorhinal cortex lesions on olfactory learning and memory in a successive-cue, go-no-go task. Behav Neurosci 105: 111-119. CrossRef
84. Panja D, Bramham CR (2014) BDNF mechanisms in late LTP formation: a synthesis and breakdown. Neuropharmacology 76: 664-676. CrossRef Medline
85. Park JJ, Loh YP (2008) How peptide hormone vesicles are transported to the secretion site for exocytosis. Mol Endocrinol 22: 2583-2595. CrossRef Medline
86. 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. Medline
87. Piomelli D (2014) More surprises lying ahead. The endocannabinoids keep us guessing. Neuropharmacology 76: 228-234. CrossRef Medline
88. Ratano P, Everitt BJ, Milton AL (2014) The CB1 receptor antagonist AM251 impairs reconsolidation of pavlovian fear memory in the rat basolateral amygdala. Neuropsychopharmacology 39: 2529-2537. CrossRef Medline
89. Reagh ZM, Yassa MA (2014) Object and spatial mnemonic interference differentially engage lateral and medial entorhinal cortex in humans. Proc Natl Acad Sci U S A 111: E4264-E4273. CrossRef Medline
90. Rex CS, Lin CY, Kramár EA, Chen LY, Gall CM, Lynch G (2007) Brain-derived neurotrophic factor promotes long-term potentiationrelated cytoskeletal changes in adult hippocampus. J Neurosci 27: 3017-3029. CrossRef Medline
91. Rodriguez A, Laio A (2014) Machine learning. Clustering by fast search and find of density peaks. Science 344: 1492-1496. Cross-Ref Medline
92. Roland AB, Ricobaraza A, Carrel D, Jordan BM, Rico F, Simon A, Humbert-Claude M, Ferrier J, McFadden MH, Scheuring S, Lenkei Z (2014) Cannabinoid-induced actomyosin contractility shapes neuronal morphology and growth. Elife 3: e03159. CrossRef Medline
93. Rudy JW (2015) Actin dynamics and the evolution of the memory trace. Brain Res 1621: 17-28. CrossRef Medline
94. Sankaranarayanan S, Atluri PP, Ryan TA (2003) Actin has a molecular scaffolding, not propulsive, role in presynaptic function. Nat Neurosci 6: 127-135. CrossRef Medline
95. Santana F, Sierra RO, Haubrich J, Crestani AP, Duran JM, de Freitas Cassini L, de Oliveira Alvares L, Quillfeldt JA (2016) Involvement of the infralimbic cortex and CA1 hippocampal area in reconsolidation of a contextual fear memory through CB1 receptors: effects of CP55,940. Neurobiol Learn Mem 127: 42-47. CrossRef Medline
96. Schmitz SK, King C, Kortleven C, Huson V, Kroon T, Kevenaar JT, Schut D, Saarloos I, Hoetjes JP, de Wit H, Stiedl O, Spijker S, Li KW, Mansvelder HD, Smit AB, Cornelisse LN, Verhage M, Toonen RF (2016) Presynaptic inhibition upon CB1 or mGlu2/3 receptor activation requires ERK/MAPK phosphorylation of Munc18-1. EMBO J 35: 1236-1250. CrossRef Medline
97. Seese RR, Babayan AH, Katz AM, Cox CD, Lauterborn JC, Lynch G, Gall CM (2012) LTP induction translocates cortactin at distant synapses in wild-type but not Fmr1 knock-out mice. J Neurosci 32: 7403-7413. CrossRef Medline
98. Seese RR, Wang K, Yao YQ, Lynch G, Gall CM (2014) Spaced training rescues memory and ERK1/2 signaling in fragile X syndrome model mice. Proc Natl Acad Sci U S A 111: 16907-16912. CrossRef Medline
99. Sigurdsson T, Doyère V, Cain CK, LeDoux JE (2007) Long-term potentiation in the amygdala: a cellular mechanism of fear learning and memory. Neuropharmacology 52: 215-227. CrossRef Medline
100. Simmons MA, Schneider CR (1998) Regulation of M-type potassium current by intracellular nucleotide phosphates. J Neurosci 18: 6254-6260. Medline
101. Soria-Gómez E, Bellocchio L, Reguero L, Lepousez G, Martin C, Bendahmane M, Ruehle S, Remmers F, Desprez T, Matias I, Wiesner T, Cannich A, Nissant A, Wadleigh A, Pape HC, Chiarlone AP, Quarta C, Verrier D, Vincent P, Massa F, Lutz B, Guzmán M, Gurden H, Ferreira G, Lledo PM, Grandes P, Marsicano G (2014) The endocannabinoid system controls food intake via olfactory processes. Nat Neurosci 17: 407-415. CrossRef Medline
102. Stäubli U, Ivy G, Lynch G (1984) Hippocampal denervation causes rapid forgetting of olfactory information in rats. Proc Natl Acad Sci U S A 81: 5885-5887. Medline
103. Stäubli U, Larson J, Lynch G (1990) Mossy fiber potentiation and long-term potentiation involve different expression mechanisms. Synapse 5: 333-335. CrossRef Medline
104. Sugaya Y, Cagniard B, Yamazaki M, Sakimura K, Kano M (2013) The endocannabinoid 2-arachidonoylglycerol negatively regulates habituation by suppressing excitatory recurrent network activity and reducing long-term potentiation in the dentate gyrus. J Neurosci 33: 3588-3601. CrossRef Medline
105. Tan H, Ahmad T, Loureiro M, Zunder J, Laviolette SR (2014) The role of cannabinoid transmission in emotional memory formation: implications for addiction and schizophrenia. Front Psychiatry 5: 73 CrossRef Medline
106. Tart CT (1970) Marijuana intoxication common experiences. Nature 226: 701-704. Medline
107. Trieu BH, Kramár EA, Cox CD, Jia Y, Wang W, Gall CM, Lynch G (2015) Pronounced differences in signal processing and synaptic plasticity between piriform-hippocampal network stages: a prominent role for adenosine. J Physiol 593: 2889-2907. CrossRef Medline
108. Uchigashima M, Yamazaki M, Yamasaki M, Tanimura A, Sakimura K, Kano M, Watanabe M (2011) Molecular and morphological configuration for 2-arachidonoylglycerol-mediated retrograde signaling at mossy cell-granule cell synapses in the dentate gyrus. J Neurosci 31: 7700-7714. CrossRef Medline
109. van Groen T, Miettinen P, Kadish I (2003) The entorhinal cortex of the mouse: organization of the projection to the hippocampal formation. Hippocampus 13: 133-149. CrossRef Medline
110. Wigström H, Gustafsson B (1986) Postsynaptic control of hippocampal long-term potentiation. J Physiol (Paris) 81: 228-236. Medline
111. Wilson DI, Watanabe S, Milner H, Ainge JA (2013) Lateral entorhinal cortex is necessary for associative but not nonassociative recognition memory. Hippocampus 23: 1280-1290. CrossRef Medline
112. Witter MP (1993) Organization of the entorhinal-hippocampal system: a review of current anatomical data. Hippocampus 3: 33-44.
113. Witter MP, Wouterlood FG, Naber PA, Van Haeften T (2000) Anatomical organization of the parahippocampal-hippocampal network. Ann N Y Acad Sci 911: 1-24. Medline
114. Xu JY, Zhang J, Chen C (2012) Long-lasting potentiation of hippocampal synaptic transmission by direct cortical input is mediated via endocannabinoids. J Physiol 590: 2305-2315. CrossRef Medline