Neurotrophins play differential roles in short and long-term recognition memory

Neurobiology of Learning and Memory

Volumn 104, Issue , 2013, Pages 39-48

  Callaghan, Charlotte K ^a   Kelly, Áine M ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

BDNF; Dentate gyrus; Learning; Memory; Neurotrophin; Perirhinal cortex

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; NERVE GROWTH FACTOR; NEUROTROPHIN; NEUROTROPHIN 3; NEUROTROPHIN 4; NEUTRALIZING ANTIBODY; TYROSINE KINASE RECEPTOR; TYRPHOSTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; DENTATE GYRUS; HIPPOCAMPUS; LONG TERM MEMORY; MALE; MEMORY DISORDER; NONHUMAN; PERIRHINAL CORTEX; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SHORT TERM MEMORY; SYNAPTIC TRANSMISSION; TASK PERFORMANCE;

BDNF; DENTATE GYRUS; LEARNING; MEMORY; NEUROTROPHIN; PERIRHINAL CORTEX;

ANIMALS; ANTIBODIES, BLOCKING; BRAIN-DERIVED NEUROTROPHIC FACTOR; CEREBRAL CORTEX; MALE; MEMORY, LONG-TERM; MEMORY, SHORT-TERM; NERVE GROWTH FACTOR; NERVE GROWTH FACTORS; NEUROTROPHIN 3; RATS; RATS, WISTAR; RECEPTOR PROTEIN-TYROSINE KINASES; RECOGNITION (PSYCHOLOGY); TYRPHOSTINS;

EID: 84878734436     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2013.04.011     Document Type: Article

References (81)

1. Aicardi G., Argilli E., Cappello S., Santi S., Riccio M., Thoenen H., et al. Induction of long-term potentiation and depression is reflected by corresponding changes in secretion of endogenous brain-derived neurotrophic factor [In Vitro Research Support, Non-U.S. Gov't]. Proceedings of the National Academy of Sciences USA 2004, 101(44):15788-15792. 10.1073/pnas.0406960101.
2. Alonso M., Bekinschtein P., Cammarota M., Vianna M.R., Izquierdo I., Medina J.H. Endogenous BDNF is required for long-term memory formation in the rat parietal cortex [Comparative Study Research Support, Non-U.S. Gov't]. Learning and Memory 2005, 12(5):504-510. 10.1101/lm.27305.
3. Alonso M., Vianna M.R., Depino A.M., Mello e Souza T., Pereira P., Szapiro G., et al. BDNF-triggered events in the rat hippocampus are required for both short- and long-term memory formation [Research Support, Non-U.S. Gov't]. Hippocampus 2002, 12(4):551-560. doi: 10.1002/hipo.10035.
4. Asztely F., Kokaia M., Olofsdotter K., Ortegren U., Lindvall O. Afferent-specific modulation of short-term synaptic plasticity by neurotrophins in dentate gyrus [Comparative Study Research Support, Non-U.S. Gov't]. European Journal of Neuroscience 2000, 12(2):662-669.
5. Balderas I., Rodriguez-Ortiz C.J., Salgado-Tonda P., Chavez-Hurtado J., McGaugh J.L., Bermudez-Rattoni F. The consolidation of object and context recognition memory involve different regions of the temporal lobe [Research Support, Non-U.S. Gov't]. Learning and Memory 2008, 15(9):618-624. 10.1101/lm.1028008.
6. Bekinschtein P., Cammarota M., Igaz L.M., Bevilaqua L.R., Izquierdo I., Medina J.H.( Persistence of long-term memory storage requires a late protein synthesis- and BDNF- dependent phase in the hippocampus [Research Support, Non-U.S. Gov't]. Neuron 2007, 53(2):261-277. doi: 10.1016/j.neuron.2006.11.025.
7. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus [Review]. Nature 1993, 361(6407):31-39. 10.1038/361031a0.
8. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding [Research Support, U.S. Gov't, P.H.S.]. Analytical Biochemistry 1976, 72:248-254.
9. Bramham C.R., Southard T., Sarvey J.M., Herkenham M., Brady L.S. Unilateral LTP triggers bilateral increases in hippocampal neurotrophin and trk receptor mRNA expression in behaving rats: Evidence for interhemispheric communication [Research Support, U.S. Gov't, P.H.S.]. Journal of Comparative Neurology 1996, 368(3):371-382. doi: 10.1002/(SICI)1096-9861(19960506)368:3<371::AID-CNE4>3.0.CO;2-2.
10. Brown M.W., Aggleton J.P. Recognition memory: What are the roles of the perirhinal cortex and hippocampus? [Research Support, Non-U.S. Gov't Review]. Nature Reviews Neuroscience 2001, 2(1):51-61. 10.1038/35049064.
11. Callaghan C.K., Kelly A.M. Differential BDNF signaling in dentate gyrus and perirhinal cortex during consolidation of recognition memory in the rat [Research Support, Non-U.S. Gov't]. Hippocampus 2012, 22(11):2127-2135. 10.1002/hipo.22033.
12. Castren E., Pitkanen M., Sirvio J., Parsadanian A., Lindholm D., Thoenen H., et al. The induction of LTP increases BDNF and NGF mRNA but decreases NT-3 mRNA in the dentate gyrus. NeuroReport 1993, 4(7):895-898.
13. Chen J., Kitanishi T., Ikeda T., Matsuki N., Yamada M.K. Contextual learning induces an increase in the number of hippocampal CA1 neurons expressing high levels of BDNF [Research Support, Non-U.S. Gov't]. Neurobiology of Learning and Memory 2007, 88(4):409-415. 10.1016/j.nlm.2007.07.009.
14. Chen G., Kolbeck R., Barde Y.A., Bonhoeffer T., Kossel A. Relative contribution of endogenous neurotrophins in hippocampal long-term potentiation [In Vitro Research Support, Non-U.S. Gov't]. Journal of Neuroscience 1999, 19(18):7983-7990.
15. Chen L.Y., Rex C.S., Pham D.T., Lynch G., Gall C.M. BDNF signaling during learning is regionally differentiated within hippocampus [Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.]. Journal of Neuroscience 2010, 30(45):15097-15101. 10.1523/JNEUROSCI.3549-10.2010.
16. Clarke R.P. Does longer-term memory storage never become overloaded, and would such overload cause Alzheimer's disease and other dementia?. Medical Hypotheses 2000, 55(5):419-428. 10.1054/mehy.2000.1082.
17. Davis C.B., Hepburn T.W., Urbanski J.J., Kwok D.C., Hart T.K., Herzyk D.J., et al. Preclinical pharmacokinetic evaluation of the respiratory syncytial virus-specific reshaped human monoclonal antibody RSHZ19. Drug Metabolism and Disposition 1995, 23(10):1028-1036.
18. de Lima M.N., Luft T., Roesler R., Schroder N. Temporary inactivation reveals an essential role of the dorsal hippocampus in consolidation of object recognition memory [Research Support, Non-U.S. Gov't]. Neuroscience Letters 2006, 405(1-2):142-146. 10.1016/j.neulet.2006.06.044.
19. De Rosa R., Garcia A.A., Braschi C., Capsoni S., Maffei L., Berardi N., et al. Intranasal administration of nerve growth factor (NGF) rescues recognition memory deficits in AD11 anti-NGF transgenic mice [Research Support, Non-U.S. Gov't]. Proceedings of the National Academy of Sciences USA 2005, 102(10):3811-3816. 10.1073/pnas.0500195102.
20. Diogenes M.J., Costenla A.R., Lopes L.V., Jeronimo-Santos A., Sousa V.C., Fontinha B.M., et al. Enhancement of LTP in aged rats is dependent on endogenous BDNF [Research Support, Non-U.S. Gov't]. Neuropsychopharmacology 2011, 36(9):1823-1836. 10.1038/npp.2011.64.
21. Dudai Y., Eisenberg M. Rites of passage of the engram: Reconsolidation and the lingering consolidation hypothesis [Review]. Neuron 2004, 44(1):93-100. doi: 10.1016/j.neuron.2004.09.003.
22. Eisinger D.A., Ammer H. Delta-Opioid receptors stimulate ERK1/2 activity in NG108-15 hybrid cells by integrin-mediated transactivation of TrkA receptors. FEBS Letters 2008, 582(23-24):3325-3329. 10.1016/j.febslet.2008.08.021.
23. Elliott R.C., Gall C.M. Changes in activating protein 1 (AP-1) composition correspond with the biphasic profile of nerve growth factor mRNA expression in rat hippocampus after hilus lesion-induced seizures [Research Support, U.S. Gov't, P.H.S.]. Journal of Neuroscience 2000, 20(6):2142-2149.
24. Ennaceur A., Delacour J. A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data [Research Support, Non-U.S. Gov't]. Behavioural Brain Research 1988, 31(1):47-59.
25. Ennaceur A., Neave N., Aggleton J.P. Neurotoxic lesions of the perirhinal cortex do not mimic the behavioural effects of fornix transection in the rat [Research Support, Non-U.S. Gov't]. Behavioural Brain Research 1996, 80(1-2):9-25.
26. Garcia R.L., Sadighi M., Francis S.M., Suttie J.M., Fleming J.S. Expression of neurotrophin-3 in the growing velvet antler of the red deer Cervus elaphus. Journal of Molecular Endocrinology 1997, 19(2):173-182.
27. Gaskin S., Tardif M., Cole E., Piterkin P., Kayello L., Mumby D.G. Object familiarization and novel-object preference in rats [Research Support, Non-U.S. Gov't]. Behavioural Processes 2010, 83(1):61-71. 10.1016/j.beproc.2009.10.003.
28. Gooney M., Lynch M.A. Long-term potentiation in the dentate gyrus of the rat hippocampus is accompanied by brain-derived neurotrophic factor-induced activation of TrkB [Research Support, Non-U.S. Gov't]. Journal of Neurochemistry 2001, 77(5):1198-1207.
29. Gooney M., Shaw K., Kelly A., O'Mara S.M., Lynch M.A. Long-term potentiation and spatial learning are associated with increased phosphorylation of TrkB and extracellular signal-regulated kinase (ERK) in the dentate gyrus: Evidence for a role for brain-derived neurotrophic factor [Research Support, Non-U.S. Gov't]. Behavioral Neuroscience 2002, 116(3):455-463.
30. Griffin E.W., Bechara R.G., Birch A.M., Kelly A.M. Exercise enhances hippocampal-dependent learning in the rat: Evidence for a BDNF-related mechanism [Research Support, Non-U.S. Gov't]. Hippocampus 2009, 19(10):973-980. 10.1002/hipo.20631.
31. Haan E.A., Bowen D.M. Protection of neocortical tissue prisms from freeze-thaw injury by dimethyl sulphoxide [Research Support, Non-U.S. Gov't]. Journal of Neurochemistry 1981, 37(1):243-246.
32. Hagihara H., Hara M., Tsunekawa K., Nakagawa Y., Sawada M., Nakano K. Tonic-clonic seizures induce division of neuronal progenitor cells with concomitant changes in expression of neurotrophic factors in the brain of pilocarpine-treated mice [Comparative Study]. Brain Research. Molecular Brain Research 2005, 139(2):258-266. 10.1016/j.molbrainres.2005.05.031.
33. Hall J., Thomas K.L., Everitt B.J. Rapid and selective induction of BDNF expression in the hippocampus during contextual learning [Research Support, Non-U.S. Gov't]. Nature Neuroscience 2000, 3(6):533-535. 10.1038/75698.
34. Hashimoto T., Okuno H., Tokuyama W., Li Y.X., Miyashita Y. Expression of brain-derived neurotrophic factor, neurotrophin-3 and their receptor messenger RNAs in monkey rhinal cortex [Research Support, Non-U.S. Gov't]. Neuroscience 2000, 95(4):1003-1010.
35. Hennigan A., Callaghan C.K., Kealy J., Rouine J., Kelly A.M. Deficits in LTP and recognition memory in the genetically hypertensive rat are associated with decreased expression of neurotrophic factors and their receptors in the dentate gyrus [Research Support, Non-U.S. Gov't]. Behavioural Brain Research 2009, 197(2):371-377. 10.1016/j.bbr.2008.09.037.
36. Hennigan A., Trotter C., Kelly A.M. Lipopolysaccharide impairs long-term potentiation and recognition memory and increases p75NTR expression in the rat dentate gyrus [Research Support, Non-U.S. Gov't]. Brain Research 2007, 1130(1):158-166. 10.1016/j.brainres.2006.10.066.
37. Izquierdo I., Bevilaqua L.R., Rossato J.I., Bonini J.S., Medina J.H., Cammarota M. Different molecular cascades in different sites of the brain control memory consolidation [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Review]. Trends in Neurosciences 2006, 29(9):496-505. 10.1016/j.tins.2006.07.005.
38. Janis L.S., Glasier M.M., Martin G., Stackman R.W., Walsh T.J., Stein D.G. A single intraseptal injection of nerve growth factor facilitates radial maze performance following damage to the medial septum in rats [Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.]. Brain Research 1995, 679(1):99-109.
39. Jun K., Choi G., Yang S.G., Choi K.Y., Kim H., Chan G.C., et al. Enhanced hippocampal CA1 LTP but normal spatial learning in inositol 1,4,5-trisphosphate 3-kinase(A)-deficient mice [Research Support, Non-U.S. Gov't]. Learning and Memory 1998, 5(4-5):317-330.
40. Kandel E.R. The molecular biology of memory storage: A dialogue between genes and synapses [Research Support, Non-U. S. Gov't Research Support, U.S. Gov't, P.H.S. Review]. Brain Research 2001, 294(5544):1030-1038. doi: 10.1126/science.1067020.
41. Kang H., Schuman E.M. A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity [In Vitro Research Support, Non-U.S. Gov't]. Science 1996, 273(5280):1402-1406.
42. Katoh-Semba R., Takeuchi I.K., Inaguma Y., Ito H., Kato K. Brain-derived neurotrophic factor, nerve growth and neurotrophin-3 selected regions of the rat brain following kainic acid-induced seizure activity [Research Support, Non-U.S. Gov't]. Neuroscience Research 1999, 35(1):19-29.
43. Kawai H., Zago W., Berg D.K. Nicotinic alpha 7 receptor clusters on hippocampal GABAergic neurons: regulation by synaptic activity and neurotrophins. J Neurosci 2002, 22(18):7903-7912.
44. Kelly A., Conroy S., Lynch M.A. Evidence that nerve growth factor plays a role in long-term potentiation in the rat dentate gyrus [Research Support, Non-U.S. Gov't]. Neuropharmacology 1998, 37(4-5):561-570.
45. Kelly A., Laroche S., Davis S. Activation of mitogen-activated protein kinase/extracellular signal-regulated kinase in hippocampal circuitry is required for consolidation and reconsolidation of recognition memory [Research Support, Non-U.S. Gov't]. Journal of Neuroscience 2003, 23(12):5354-5360.
46. Khawaja F.A., Alonso A.A., Bourque C.W. Ca(2+)-dependent K(+) currents and spike-frequency adaptation in medial entorhinal cortex layer II stellate cells [In Vitro Research Support, Non-U.S. Gov't]. Hippocampus 2007, 17(12):1143-1148. 10.1002/hipo.20365.
47. Lee J.L., Everitt B.J., Thomas K.L. Independent cellular processes for hippocampal memory consolidation and reconsolidation [Research Support, Non-U.S. Gov't]. Science 2004, 304(5672):839-843. doi: 10.1126/science.1095760.
48. Lehmann H., Glenn M.J., Mumby D.G. Consolidation of object-discrimination memory is independent of the hippocampus in rats [Research Support, Non-U.S. Gov't]. Experimental Brain Research 2007, 180(4):755-764. 10.1007/s00221-007-0895-2.
49. Lindholm D., da Penha Berzaghi M., Cooper J., Thoenen H., Castren E. Brain-derived neurotrophic factor and neurotrophin-4 increase neurotrophin-3 expression in the rat hippocampus [Research Support, Non-U.S. Gov't]. International Journal of Developmental Neuroscience 1994, 12(8):745-751.
50. Lindvall O., Kokaia Z., Bengzon J., Elmer E., Kokaia M. Neurotrophins and brain insults [Research Support, Non-U.S. Gov't Review]. Trends in Neurosciences 1994, 17(11):490-496.
51. Lyall R.M., Zilberstein A., Gazit A., Gilon C., Levitzki A., Schlessinger J. Tyrphostins inhibit epidermal growth factor (EGF)-receptor tyrosine kinase activity in living cells and EGF-stimulated cell proliferation. Journal of Biological Chemistry 1989, 264(24):14503-14509.
52. Maguire C., Casey M., Kelly A., Mullany P.M., Lynch M.A. Activation of tyrosine receptor kinase plays a role in expression of long-term potentiation in the rat dentate gyrus [Research Support, Non-U.S. Gov't]. Hippocampus 1999, 9(5):519-526. doi: 10.1002/(SICI)1098-1063(1999)9:5<519::AID-HIPO5>3.0.CO;2-Y.
53. Malleret G., Alarcon J.M., Martel G., Takizawa S., Vronskaya S., Yin D., et al. Bidirectional regulation of hippocampal long-term synaptic plasticity and its influence on opposing forms of memory [Comparative Study Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.]. Journal of Neuroscience 2010, 30(10):3813-3825. 10.1523/JNEUROSCI.1330-09.2010.
54. Martinez-Serrano A., Fischer W., Soderstrom S., Ebendal T., Bjorklund A. Long-term functional recovery from age-induced spatial memory impairments by nerve growth factor gene transfer to the rat basal forebrain [Research Support, Non-U.S. Gov't]. Proceedings of the National Academy of Sciences USA 1996, 93(13):6355-6360.
55. Minichiello L., Casagranda F., Tatche R.S., Stucky C.L., Postigo A., Lewin G.R., et al. Point mutation in trkB causes loss of NT4-dependent neurons without major effects on diverse BDNF responses [Research Support, Non-U.S. Gov't]. Neuron 1998, 21(2):335-345.
56. Mizuno M., Yamada K., He J., Nakajima A., Nabeshima T. Involvement of BDNF receptor TrkB in spatial memory formation [Research Support, Non-U.S. Gov't]. Learning and Memory 2003, 10(2):108-115. 10.1101/lm.56003.
57. Mumby D.G., Piterkin P., Lecluse V., Lehmann H. Perirhinal cortex damage and anterograde object-recognition in rats after long retention intervals [Research Support, Non-U.S. Gov't]. Behavioural Brain Research 2007, 185(2):82-87. 10.1016/j.bbr.2007.07.026.
58. Mumby D.G., Tremblay A., Lecluse V., Lehmann H. Hippocampal damage and anterograde object-recognition in rats after long retention intervals [Research Support, Non-U.S. Gov't]. Hippocampus 2005, 15(8):1050-1056. 10.1002/hipo.20122.
59. Myskiw J.C., Rossato J.I., Bevilaqua L.R., Medina J.H., Izquierdo I., Cammarota M. On the participation of mTOR in recognition memory [Evaluation Studies Research Support, Non-U.S. Gov't]. Neurobiology of Learning and Memory 2008, 89(3):338-351. 10.1016/j.nlm.2007.10.002.
60. O'Callaghan R.M., Griffin E.W., Kelly A.M. Long-term treadmill exposure protects against age-related neurodegenerative change in the rat hippocampus [Research Support, Non-U.S. Gov't]. Hippocampus 2009, 19(10):1019-1029. 10.1002/hipo.20591.
61. Ohmichi M., Pang L., Ribon V., Gazit A., Levitzki A., Saltiel A.R. The tyrosine kinase inhibitor tyrphostin blocks the cellular actions of nerve growth factor. Biochemistry 1993, 32(17):4650-4658.
62. Ou L.C., Gean P.W. Regulation of amygdala-dependent learning by brain-derived neurotrophic factor is mediated by extracellular signal-regulated kinase and phosphatidylinositol-3-kinase [Comparative Study In Vitro Research Support, Non-U.S. Gov't]. Neuropsychopharmacology 2006, 31(2):287-296. 10.1038/sj.npp.1300830.
63. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, San Diego, CA.
64. 2+ entry [Research Support, Non-U S. Gov't]. Neuroscience 2004, 126(3):665-676. doi: 10.1016/j.neuroscience.2004.04.008.
65. Rattiner L.M., Davis M., French C.T., Ressler K.J. Brain-derived neurotrophic factor and tyrosine kinase receptor B involvement in amygdala-dependent fear conditioning [Research Support, Non-U.S. Gov'tResearch Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.]. Journal of Neuroscience 2004, 24(20):4796-4806. 10.1523/JNEUROSCI.5654-03.2004.
66. Rende M., Brizi E., Conner J., Treves S., Censier K., Provenzano C., et al. Nerve growth factor (NGF) influences differentiation and proliferation of myogenic cells in vitro via TrKA [In Vitro Research Support, Non-U.S. Gov't]. International Journal of Developmental Neuroscience 2000, 18(8):869-885.
67. Riedel G., Platt B., Micheau J. Glutamate receptor function in learning and memory [Review]. Behavioural Brain Research 2003, 140(1-2):1-47.
68. Romero-Granados R., Fontan-Lozano A., Delgado-Garcia J.M., Carrion A.M. From learning to forgetting: Behavioral, circuitry, and molecular properties define the different functional states of the recognition memory trace [Research Support, Non-U.S. Gov't]. Hippocampus 2010, 20(5):584-595. 10.1002/hipo.20669.
69. Rossato J.I., Bevilaqua L.R., Myskiw J.C., Medina J.H., Izquierdo I., Cammarota M. On the role of hippocampal protein synthesis in the consolidation and reconsolidation of object recognition memory. Learning and Memory 2007, 14(1):36-46. 10.1101/lm.422607.
70. Rossi C., Angelucci A., Costantin L., Braschi C., Mazzantini M., Babbini F., et al. Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment [Comparative Study Research Support, N.I.H., Intramural Research Support, Non-U.S. Gov't]. European Journal of Neuroscience 2006, 24(7):1850-1856. doi: 10.1111/j.1460-9568.2006.05059.x.
71. Seoane A., Tinsley C.J., Brown M.W. Interfering with perirhinal brain-derived neurotrophic factor expression impairs recognition memory in rats [Research Support, Non-U.S. Gov't]. Hippocampus 2011, 21(2):121-126. 10.1002/hipo.20763.
72. Smith D.M., Mizumori S.J. Hippocampal place cells, context, and episodic memory [Research Support, N.I.H., Extramural Review]. Hippocampus 2006, 16(9):716-729. 10.1002/hipo.20208.
73. Van der Zee C.E., Lourenssen S., Stanisz J., Diamond J. NGF deprivation of adult rat brain results in cholinergic hypofunction and selective impairments in spatial learning [Research Support, Non-U.S. Gov't]. European Journal of Neuroscience 1995, 7(1):160-168.
74. Winters B.D., Bartko S.J., Saksida L.M., Bussey T.J. Scopolamine infused into perirhinal cortex improves object recognition memory by blocking the acquisition of interfering object information [Research Support, Non-U.S. Gov't]. Learning and Memory 2007, 14(9):590-596. 10.1101/lm.634607.
75. Winters B.D., Forwood S.E., Cowell R.A., Saksida L.M., Bussey T.J. Double dissociation between the effects of peri-postrhinal cortex and hippocampal lesions on tests of object recognition and spatial memory: Heterogeneity of function within the temporal lobe [Comparative Study Research Support, Non-U.S. Gov't]. Journal of Neuroscience 2004, 24(26):5901-5908. 10.1523/JNEUROSCI.1346-04.2004.
76. Winters B.D., Tucci M.C., Jacklin D.L., Reid J.M., Newsome J. On the dynamic nature of the engram: Evidence for circuit-level reorganization of object memory traces following reactivation [Research Support, Non-U.S. Gov't]. Journal of Neuroscience 2011, 31(48):17719-17728. 10.1523/JNEUROSCI.2968-11.2011.
77. Woolf N.J., Milov A.M., Schweitzer E.S., Roghani A. Elevation of nerve growth factor and antisense knockdown of TrkA receptor during contextual memory consolidation [Research Support, U.S. Gov't, P.H.S.]. Journal of Neuroscience 2001, 21(3):1047-1055.
78. Xie C.W., Sayah D., Chen Q.S., Wei W.Z., Smith D., Liu X. Deficient long-term memory and long-lasting long-term potentiation in mice with a targeted deletion of neurotrophin-4 gene [Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.]. Proceedings of the National Academy of Sciences USA 2000, 97(14):8116-8121. 10.1073/pnas.140204597.
79. Zeng Y., Zhao D., Xie C.W. Neurotrophins enhance CaMKII activity and rescue amyloid-beta-induced deficits in hippocampal synaptic plasticity [Research Support, N.I.H., Extramural]. Journal of Alzheimer's Disease 2010, 21(3):823-831. 10.3233/JAD-2010-100264.
80. Zhang Y.H., Chi X.X., Nicol G.D. Brain-derived neurotrophic factor enhances the excitability of rat sensory neurons through activation of the p75 neurotrophin receptor and the sphingomyelin pathway [Research Support, N.I.H., Extramural]. Journal of Physiology 2008, 586(13):3113-3127. 10.1113/jphysiol.2008.152439.
81. Zhang H.N., Ko M.C. Seizure activity involved in the up-regulation of BDNF mRNA expression by activation of central mu opioid receptors [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't]. Neuroscience 2009, 161(1):301-310. doi: 10.1016/j.neuroscience.2009.03.020.