A specific role for hippocampal mossy fiber's zinc in rapid storage of emotional memories

Learning and Memory

Volumn 21, Issue 5, 2014, Pages 287-297

  Ceccom, Johnatan ^a   Halley, Hélène ^a   Daumas, Stéphanie ^b,c,d   Lassalle, Jean Michel ^a  

^a Université Paul Sabatier   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c and Centre National de la Recherche Scientifique Unité Mixte de Recherche 8246   (France)

^d CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMIC ACID; SODIUM CHLORIDE; ZINC; 2-AMINO-5-PHOSPHOPENTANOIC ACID; AMINO ACID RECEPTOR BLOCKING AGENT; CHELATING AGENT; DIETHYLDITHIOCARBAMIC ACID; EDETIC ACID; VALINE;

ANIMAL EXPERIMENT; ARTICLE; CONDITIONING; CONTROLLED STUDY; DENTATE GYRUS; FEAR; FREEZING; GRANULE CELL; HIPPOCAMPAL CA3 REGION; HIPPOCAMPAL MOSSY FIBER; MALE; MEMORY; MEMORY CONSOLIDATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; REINFORCEMENT; SPATIAL LEARNING; SYNAPSE VESICLE; ANALOGS AND DERIVATIVES; ANALYSIS OF VARIANCE; ANIMAL; C57BL MOUSE; CATALEPSY; CONDITIONED REFLEX; DRUG EFFECTS; EMOTION; HIPPOCAMPUS; METABOLISM; PHYSIOLOGY; TIME;

ANALYSIS OF VARIANCE; ANIMALS; CHELATING AGENTS; CONDITIONING, CLASSICAL; DITIOCARB; EDETIC ACID; EMOTIONS; EXCITATORY AMINO ACID ANTAGONISTS; FREEZING REACTION, CATALEPTIC; HIPPOCAMPUS; MALE; MEMORY; MICE; MICE, INBRED C57BL; MOSSY FIBERS, HIPPOCAMPAL; TIME FACTORS; VALINE; ZINC;

EID: 84901006912     PISSN: 10720502     EISSN: 15495485     Source Type: Journal    
DOI: 10.1101/lm.033472.113     Document Type: Article

References (94)

1. Abe K. 2001. Modulation of hippocampal long-term potentiation by the amygdala: a synaptic mechanism linking emotion and memory. Jpn J Pharmacol 86: 18-22.
2. Abe K, Niikura Y, Misawa M. 2003. The induction of long-term potentiation at amygdalo-hippocampal synapses in vivo. Biol Pharm Bull 26:1560-1562. (Pubitemid 41699635)
3. Anagnostaras SG, Gale GD, Fanselow MS. 2001. Hippocampus and contextual fear conditioning: recent controversies and advances. Hippocampus 11: 8-17.
4. Bach ME, Hawkins RD, Osman M, Kandel ER, Mayford M. 1995. Impairment of spatial but not contextual memory in CaMKII mutant mice with a selective loss of hippocampal LTP in the range of the theta frequency. Cell 81: 905-915.
5. Besser L, Chorin E, Sekler I, Silverman WF, Atkin S, Russell JT, Hershfinkel M. 2009. Synaptically released zinc triggers metabotropic signaling via a zinc-sensing receptor in the hippocampus. J Neurosci 29:2890-2901.
6. Blaabjerg M, Zimmer J. 2007. The dentate mossy fibers: structural organization, development and plasticity. Prog Brain Res 163: 85-107.
7. Blanchard RJ, Blanchard DC. 1969. Crouching as an index of fear. J Comp Physiol Psychol 67: 370-375.
8. Bliss TV, Collingridge GL. 1993. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31-39. (Pubitemid 23020772)
9. Bortolotto ZA, Lauri S, Isaac JT, Collingridge GL. 2003. Kainate receptors and the induction of mossy fibre long-term potentiation. Philos Trans R Soc Lond B Biol Sci 358: 657-666. (Pubitemid 36536695)
10. Bourtchouladze R, Abel T, Berman N, Gordon R, Lapidus K, Kandel ER. 1998. Different training procedures recruit either one or two critical periods for contextual memory consolidation, each of which requires protein synthesis and PKA. Learn Mem 5: 365-374. (Pubitemid 29115266)
11. Bourtchuladze R, Frenguelli B, Blendy J, Cioffi D, Schutz G, Silva AJ. 1994. Deficient long-term-memory in mice with a targeted mutation of the camp-responsive element-binding protein. Cell 79: 59-68.
12. Bovet D, Bovet-Nitti F, Oliverio A. 1969. Genetic aspects of learning and memory in mice. Science 163: 139-149.
13. Bramham CR, Milgram NW, Srebro B. 1991. Activation of AP5-sensitive NMDA receptors is not required to induce LTP of synaptic transmission in the lateral perforant path. Eur J Neurosci 3: 1300-1308.
14. Calandreau L, Trifilieff P, Mons N, Costes L, Marien M, Marighetto A, Micheau J, Jaffard R, Desmedt A. 2006. Extracellular hippocampal acetylcholine level controls amygdala function and promotes adaptive conditioned emotional response. J Neurosci 26: 13556-13566. (Pubitemid 46026488)
15. Ceccom J, Bouhsira E, Halley H, Daumas S, Lassalle JM. 2013. Differential needs of zinc in the CA3 area of dorsal hippocampus for the consolidation of contextual fear and spatial memories. Learn Mem 20:348-351.
16. Cerasti E, Treves A. 2010. How informative are spatial CA3 representations established by the dentate gyrus? PLoS Comput Biol 6: e1000759.
17. Cerasti E, Treves A. 2013. The spatial representations acquired in CA3 by self-organizing recurrent connections. Front Cell Neurosci 7: 112.
18. Cole TB, Wenzel HJ, Kafer KE, Schwartzkroin PA, Palmiter RD. 1999. Elimination of zinc from synaptic vesicles in the intact mouse brain by disruption of the ZnT3 gene. Proc Natl Acad Sci 96: 1716-1721. (Pubitemid 29098517)
19. Commins S, Cunningham L, Harvey D, Walsh D. 2003. Massed but not spaced training impairs spatial memory. Behav Brain Res 139:215-223. (Pubitemid 36298504)
20. Daumas S, Halley H, Lassalle JM. 2004. Disruption of hippocampal CA3 network: effects on episodic-like memory processing in C57BL/6J mice. Eur J Neurosci 20: 597-600. (Pubitemid 38969647)
21. Daumas S, Halley H, Frances B, Lassalle JM. 2005. Encoding, consolidation and retrieval of contextual memory: differential involvement of CA3 and CA1 hippocampal subregions. Learn Mem 12: 375-382. (Pubitemid 41126850)
22. Daumas S, Betourne A, Halley H,Wolfer DP, Lipp HP, Lassalle JM, Frances B. 2007. Transient activation of the CA3 k opioid system in the dorsal hippocampus modulates complex memory processing in mice. Neurobiol Learn Mem 88: 94-103. (Pubitemid 46809805)
23. Daumas S, Ceccom J, Halley H, Frances B, Lassalle JM. 2009. Activation of metabotropic glutamate receptor type 2/3 supports the involvement of the hippocampal mossy fiber pathway on contextual fear memory consolidation. Learn Mem 16: 504-507.
24. Diamond DM, Campbell AM, Park CR, Halonen J, Zoladz PR. 2007. The temporal dynamics model of emotional memory processing: a synthesis on the neurobiological basis of stress-induced amnesia, flashbulb and traumatic memories, and the Yerkes-Dodson law. Neural Plast 2007: 60803.
25. Fanselow MS, Kim JJ, Decola JP, Landeirafernandez J. 1990. Blockade of Pavlovian fear conditioning by the NMDA antagonist. Bull Psychon Soc 28: 527-528.
26. Fellini L, Florian C, Courtey J, Roullet P. 2009. Pharmacological intervention of hippocampal CA3 NMDA receptors impairs acquisition and long-term memory retrieval of spatial pattern completion task. Learn Mem 16: 387-394.
27. Florian C, Roullet P. 2004. Hippocampal CA3-region is crucial for acquisition and memory consolidation in Morris water maze task in mice. Behav Brain Res 154: 365-374. (Pubitemid 39093987)
28. Frederickson R, Frederickson CJ, Danscher G. 1990. In situ binding of bouton zinc reversibly disrupts performance on a spatial memory task. Behav Brain Res 38: 25-33. (Pubitemid 20139573)
29. Gundelfinger ED, Boeckers TM, Baron MK, Bowie JU. 2006. A role for zinc in postsynaptic density asSAMbly and plasticity? Trends Biochem Sci 31:366-373.
30. Hu H, Real E, Takamiya K, Kang MG, Ledoux J, Huganir RL, Malinow R. 2007. Emotion enhances learning via norepinephrine regulation of AMPA-receptor trafficking. Cell 131: 160-173. (Pubitemid 47498536)
31. Huang YY, Kandel ER. 1996. Modulation of both the early and the late phase of mossy fiber LTP by the activation of b-adrenergic receptors. Neuron 16: 611-617. (Pubitemid 26101111)
32. Huang YZ, Pan E, Xiong ZQ, McNamara JO. 2008. Zinc-mediated transactivation of TrkB potentiates the hippocampal mossy fiber-CA3 pyramid synapse. Neuron 57: 546-558. (Pubitemid 351273988)
33. Hubbard SR, Bishop WR, Kirschmeier P, George SJ, Cramer SP, Hendrickson WA. 1991. Identification and characterization of zinc binding sites in protein kinase C. Science 254: 1776-1779. (Pubitemid 21917523)
34. Ikegaya Y, Nakanishi K, Saito H, Abe K. 1997. Amygdala b-noradrenergic influence on hippocampal long-term potentiation in vivo. Neuroreport 8: 3143-3146. (Pubitemid 27421747)
35. Ikegaya Y, Delcroix I, Iwakura Y, Matsuki N, Nishiyama N. 2003. Interleukin-1b abrogates long-term depression of hippocampal CA1 synaptic transmission. Synapse 47: 54-57. (Pubitemid 35424543)
36. Izumi Y, Auberson YP, Zorumski CF. 2006. Zinc modulates bidirectional hippocampal plasticity by effects on NMDA receptors. J Neurosci 26:7181-7188.
37. Kerr AM, Jonas P. 2008. The two sides of hippocampal mossy fiber plasticity. Neuron 57: 5-7.
38. Kogan JH, Frankland PW, Blendy JA, Coblentz J, Marowitz Z, Schutz G, Silva AJ. 1997. Spaced training induces normal long-term memory in CREB mutant mice. Curr Biol 7: 1-11. (Pubitemid 27058935)
39. Koh J, Suh S, Gwag B, He Y, Hsu C, Choi D. 1996. The role of zinc in selective neuronal death after transient global cerebral ischemia. Science 272:1013-1016. (Pubitemid 26259319)
40. Kuriyama K, Soshi T, Fujii T, Kim Y. 2010. Emotional memory persists longer than event memory. Learn Mem 17: 130-133.
41. Kwon HB, Castillo PE. 2008. Long-term potentiation selectively expressed by NMDA receptors at hippocampal mossy fiber synapses. Neuron 57:108-120.
42. Lassalle JM, Bataille T, Halley H. 2000. Reversible inactivation of the hippocampal mossy fiber synapses in mice impairs spatial learning, but neither consolidation nor memory retrieval, in the Morris navigation task. Neurobiol Learn Mem 73: 243-257. (Pubitemid 30250104)
43. Lee JC, Hynds RE. 2013. Divergent cellular pathways of hippocampal memory consolidation and reconsolidation. Hippocampus 23: 233-244.
44. Lee JLC, Everitt BJ, Thomas KL. 2004. Independent cellular processes for hippocampal memory consolidation and reconsolidation. Science 304:839-843. (Pubitemid 38620176)
45. Lehmann H, McNamara KC. 2011. Repeatedly reactivated memories become more resistant to hippocampal damage. Learn Mem 18:132-135.
46. Lengyel I, Fieuw-Makaroff S, Hall AL, Sim ATR, Rostas JAP, Dunkley PR. 2000. Modulation of the phosphorylation and activity of calcium/calmodulin- dependent protein kinase II by zinc. J Neurochem 75:594-605. (Pubitemid 30485440)
47. Li Y, Hough CJ, Frederickson CJ, Sarvey JM. 2001a. Induction of mossy fiber CA3 long-term potentiation requires translocation of synaptically released Zn2+. J Neurosci 21: 8015-8025. (Pubitemid 32952758)
48. Li Y, Hough CJ, Suh SW, Sarvey JM, Frederickson CJ. 2001b. Rapid translocation of Zn2+ from presynaptic terminals into postsynaptic hippocampal neurons after physiological stimulation. J Neurophysiol 86: 2597-2604. (Pubitemid 34000617)
49. Li YV, Hough CJ, Sarvey JM. 2003. Do we need zinc to think? Science stke. 182: pe19. doi: 10.1126/stke.2003.182.pe19.
50. Linkous DH, Flinn JM, Koh JY, Lanzirotti A, Bertsch PM, Jones BF, Giblin LJ, Frederickson CJ. 2008. Evidence that the ZnT3 protein controls the total amount of elemental zinc in synaptic vesicles. J Histochem Cytochem 56: 3-6. (Pubitemid 350276496)
51. Lisman JE. 1999. Relating hippocampal circuitry to function: recall of memory sequences by reciprocal dentate-CA3 interactions. Neuron 22:233-242. (Pubitemid 29109658)
52. 2+ is required for the induction of long-term potentiation at rat hippocampal mossy fiber-CA3 synapses. Synapse 38: 187-197.
53. Malherbe P, Richards JG, Broger C, Zenner MT, Messer J, Kratzeisen C, Nakanishi S, Mutel V. 2005. Opposite effects of Zn on the in vitro binding of [3H]LY354740 to recombinant and native metabotropic glutamate 2 and 3 receptors. J Neurochem 94: 150-160.
54. Manzerra P, Behrens MM, Canzoniero LMT, Wang XQ, Heidinger V, Ichinose T, Yu SP, Choi DW. 2001. Zinc induces a Src family kinase-mediated up-regulation of NMDA receptor activity and excitotoxicity. Proc Natl Acad Sci 98: 11055-11061. (Pubitemid 32928682)
55. Marr D. 1971. Simple memory: a theory for archicortex. Philos Trans R Soc Lond B Biol Sci 262: 23-81.
56. Martel G, Hevi C, Friebely O, Baybutt T, Shumyatsky GP. 2010. Zinc transporter 3 is involved in learned fear and extinction, but not in innate fear. Learn Mem 17: 582-590.
57. McNaughton N, Morris RG. 1987. Chlordiazepoxide, an anxiolytic benzodiazepine, impairs place navigation in rats. Behav Brain Res 24:39-46. (Pubitemid 17056352)
58. Nakao K, Matsuyama K, Matsuki N, Ikegaya Y. 2004. Amygdala stimulation modulates hippocampal synaptic plasticity. Proc Natl Acad Sci 101:14270-14275. (Pubitemid 39305064)
59. Nakazawa K, Sun LD, Quirk MC, Rondi-Reig L, Wilson MA, Tonegawa S. 2003. Hippocampal CA3 NMDA receptors are crucial for memory acquisition of one-time experience. Neuron 38: 305-315. (Pubitemid 36555655)
60. Nicoll RA, Schmitz D. 2005. Synaptic plasticity at hippocampal mossy fibre synapses. Nat Rev Neurosci 6: 863-876. (Pubitemid 41568728)
61. O'Keefe J, Dostrovsky J. 1971. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34: 171-175.
62. Overduin SA, Richardson AG, Lane CE, Bizzi E, Press DZ. 2006. Intermittent practice facilitates stable motor memories. J Neurosci 26: 11888-11892. (Pubitemid 44772099)
63. Park JA, Koh JY. 1999. Induction of an immediate early gene egr-1 by zinc through extracellular signal-regulated kinase activation in cortical culture: Its role in zinc-induced neuronal death. J Neurochem 73:450-456. (Pubitemid 29339816)
64. Paxinos G, Franklin KBJ. 2001. The mouse brain in stereotaxic coordinates. Academic Press, San Diego, CA.
65. Phillips RG, Ledoux JE. 1992. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 106: 274-285.
66. Pinheiro PS, Mulle C. 2008. Presynaptic glutamate receptors: physiological functions and mechanisms of action. Nat Rev Neurosci 9: 423-436.
67. Rebola N, Lujan R, Cunha RA, Mulle C. 2008. Adenosine A2A receptors are essential for long-term potentiation of NMDA-EPSCs at hippocampal mossy fiber synapses. Neuron 57: 121-134.
68. Rolls ET. 2007. An attractor network in the hippocampus: theory and neurophysiology. Learn Mem 14: 714-731. (Pubitemid 350172771)
69. Scharf MT,WooNH, Lattal KM, Young JZ, Nguyen PV, Abel T. 2002. Protein synthesis is required for the enhancement of long-term potentiation and long-term memory by spaced training. J Neurophysiol 87:2770-2777. (Pubitemid 34670656)
70. Schildt S, Endres T, Lessmann V, Edelmann E. 2013. Acute and chronic interference with BDNF/TrkB-signaling impair LTP selectively at mossy fiber synapses in the CA3 region of mouse hippocampus. Neuropharmacol 71: 247-254.
71. Schmitz D, Mellor J, Nicoll RA. 2001. Presynaptic kainate receptor mediation of frequency facilitation at hippocampal mossy fiber synapses. Science 291: 1972-1976. (Pubitemid 32216999)
72. Sensi SL, Paoletti P, Bush AI, Sekler I. 2009. Zinc in the physiology and pathology of the CNS. Nat Rev Neurosci 10: 780-792.
73. Sensi SL, Paoletti P, Koh JY, Aizenman E, Bush AI, Hershfinkel M. 2011. The neurophysiology and pathology of brain zinc. J Neurosci 31:16076-16085.
74. Shigemoto R, Kinoshita A,Wada E, Nomura S, Ohishi H, Takada M, Flor PJ, Neki A, Abe T, Nakanishi S, et al. 1997. Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J Neurosci 17: 7503-7522. (Pubitemid 27413281)
75. Sigurdsson T, Doyere V, Cain CK, LeDoux JE. 2007. Long-term potentiation in the amygdala: a cellular mechanism of fear learning and memory. Neuropharmacol 52: 215-227. (Pubitemid 46026826)
76. Sindreu CB, Varoqui H, Erickson JD, Perez-Clausell J. 2003. Boutons containing vesicular zinc define a subpopulation of synapses with low AMPAR content in rat hippocampus. Cereb Cortex 13: 823-829. (Pubitemid 36917961)
77. Sindreu C, Palmiter RD, Storm DR. 2011. Zinc transporter ZnT-3 regulates presynaptic Erk1/2 signaling and hippocampus-dependent memory. Proc Natl Acad Sci 108: 3366-3370.
78. 2+ ions: modulators of excitatory and inhibitory synaptic activity. Neuroscientist 10: 432-442. (Pubitemid 39244580)
79. Stupien G, Florian C, Roullet P. 2003. Involvement of the hippocampal CA3-region in acquisition and in memory consolidation of spatial but not in object information in mice. Neurobiol Learn Mem 80: 32-41. (Pubitemid 36539436)
80. Sudhof TC. 1995. The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 375: 645-653.
81. Takeda A, Sawashita J, Takefuta S, Ohnuma M, Okada S. 1999. Role of zinc released by stimulation in rat amygdala. J Neurosci Res 57: 405-410. (Pubitemid 29339797)
82. Takeda A, Minami A, Seki Y, Oku N. 2004. Differential effects of zinc on glutamatergic and GAB Aergic neurotransmitter systems in the hippocampus. J Neurosci Res 75: 225-229. (Pubitemid 38049393)
83. Takeda A, Nakajima S, Fuke S, Sakurada N, Minami A, Oku N. 2006. Zinc release from Schaffer collaterals and its significance. Brain Res Bull 68:442-447. (Pubitemid 43177580)
84. Takeda A, Fuke S, Minami A, Oku N. 2007. Role of zinc influx via AMPA/kainate receptor activation in metabotropic glutamate receptor-mediated calcium release. J Neurosci Res 85: 1310-1317. (Pubitemid 46724374)
85. Takeda A, Fuke S, Ando M, Oku N. 2008a. Positive modulation of long-term potentiation at hippocampal CA1 synapses by low micromolar concentrations of zinc. Neurosci 158: 585-591.
86. Takeda A, Kanno S, Sakurada N, Ando M, Oku N. 2008b. Attenuation of hippocampal mossy fiber long-term potentiation by low micromolar concentrations of zinc. J Neurosci Res 86: 2906-2911.
87. Takeda A, Sakurada N, Ando M, Kanno S, Oku N. 2009. Facilitation of zinc influx via AMPA/kainate receptor activation in the hippocampus. Neurochem Int 55: 376-382.
88. Takeda A, Iwaki H, Ando M, Itagaki K, Suzuki M, Oku N. 2010. Zinc differentially acts on components of long-term potentiation at hippocampal CA1 synapses. Brain Res 1323: 59-64.
89. Treves A, Rolls ET. 1992. Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network. Hippocampus 2: 189-199.
90. Tully K, Bolshakov VY. 2010. Emotional enhancement of memory: how norepinephrine enables synaptic plasticity. Mol Brain 3: 15. doi:10.1186/1756-6606-3-15.
91. 2+ spillover modulates heterosynaptic N-methyl-D-aspartate receptor activity in hippocampal CA3 circuits. J Cell Biol 158: 215-220.
92. Vogt K, Mellor J, Tong G, Nicoll R. 2000. The actions of synaptically released zinc at hippocampal mossy fiber synapses. Neuron 26:187-196.
93. Wiltgen BJ, Zhou M, Cai Y, Balaji J, Karlsson MG, Parivash SN, Li WD, Silvaz AJ. 2010. The hippocampus plays a selective role in the retrieval of detailed contextual memories. Curr Biol 20: 1336-1344.
94. Yeckel MF, Kapur A, Johnston D. 1999. Multiple forms of LTP in hippocampal CA3 neurons use a common postsynaptic mechanism. Nat Neurosci 2: 625-633. (Pubitemid 30491213)