Restoration of synaptic plasticity and learning in young and aged NCAM-deficient mice by enhancing neurotransmission mediated by GluN2A-containing NMDA receptors

Journal of Neuroscience

Volumn 32, Issue 7, 2012, Pages 2263-2275

  Kochlamazashvili, Gaga ^a,b   Bukalo, Olena ^a   Senkov, Oleg ^a,c   Salmen, Benedikt ^a   Gerardy Schahn, Rita ^d   Engel, Andreas K ^a   Schachner, Melitta ^a,e,f   Dityatev, Alexander ^a,b,g  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d HANNOVER MEDICAL SCHOOL   (Germany)

^e RUTGERS UNIVERSITY   (United States)

^f SHANTOU UNIVERSITY MEDICAL COLLEGE   (China)

^g LOBACHEVSKY STATE UNIVERSITY OF NIZHNY NOVGOROD   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CYCLOSERINE; MAGNESIUM ION; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; NERVE CELL ADHESION MOLECULE; POLYSIALIC ACID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CONDITIONING; CONTROLLED STUDY; FEAR; FEMALE; HIPPOCAMPUS; LEARNING; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; MEMORY; MOUSE; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; SCHIZOPHRENIA; SYNAPTIC TRANSMISSION;

AGE FACTORS; AGING; ANIMALS; CYCLOSERINE; HIPPOCAMPUS; LEARNING; LONG-TERM POTENTIATION; MALE; MICE; MICE, KNOCKOUT; NEURAL CELL ADHESION MOLECULES; NEURAL INHIBITION; NEURONAL PLASTICITY; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84857087536     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5103-11.2012     Document Type: Article

References (103)

1. Abrous DN, Montaron MF, Petry KG, Rougon G, Darnaudéry M, Le Moal M, Mayo W (1997) Decrease in highly polysialylated neuronal cell adhesion molecules and in spatial learning during ageing are not correlated. Brain Res 744:285-292.
2. Aniksztejn L, Ben-Ari Y (1991) Novel form of long-term potentiation produced by a K+ channel blocker in the hippocampus. Nature 349:67-69.
3. Aura J, Riekkinen P Jr (2000) Pre-training blocks the improving effect of tetrahydroaminoacridine and D-cycloserine on spatial navigation performance in aged rats. Eur J Pharmacol 390:313-318.
4. Aura J, Riekkinen M, Riekkinen P Jr (1998) Tetrahydroaminoacridine and D-cycloserine stimulate acquisition of water maze spatial navigation in aged rats. Eur J Pharmacol 342:15-20.
5. Bado P, Madeira C, Vargas-Lopes C, Moulin TC, Wasilewska-Sampaio AP, Maretti L, de Oliveira RV, Amaral OB, Panizzutti R (2011) Effects of low-dose D-serine on recognition and working memory in mice. Psychopharmacology 218:461-470.
6. Barbeau D, Liang JJ, Robitalille Y, Quirion R, Srivastava LK (1995) Decreased expression of the embryonic form of the neural cell adhesion molecule in schizophrenic brains. Proc Natl Acad Sci U S A 92:2785-2789.
7. Barnes CA, Rao G, Shen J (1997) Age-related decrease in the N-methyl-DaspartateR- mediated excitatory postsynaptic potential in hippocampal region CA1. Neurobiol Aging 18:445-452.
8. Bartlett TE, Bannister NJ, Collett VJ, Dargan SL, Massey PV, Bortolotto ZA, Fitzjohn SM, Bashir ZI, Collingridge GL, Lodge D (2007) Differential roles of NR2A and NR2B-containing NMDA receptors in LTP and LTD in the CA1 region of two-week old rat hippocampus. Neuropharmacology 52:60-70.
9. Battaglia F, Wang HY, Ghilardi MF, Gashi E, Quartarone A, Friedman E, Nixon RA (2007) Cortical plasticity in Alzheimer's disease in humans and rodents. Biol Psychiatry 62:1405-1412.
10. Baxter MG, Lanthorn TH, Frick KM, Golski S, Wan RQ, Olton DS (1994) D-cycloserine, a novel cognitive enhancer, improves spatial memory in aged rats. Neurobiol Aging 15:207-213.
11. Becker CG, Artola A, Gerardy-Schahn R, Becker T, Welzl H, Schachner M (1996) The polysialic acid modification of the neural cell adhesion molecule is involved in spatial learning and hippocampal long-term potentiation. J Neurosci Res 45:143-152.
12. Billard JM, Rouaud E (2007) Deficit of NMDA receptor activation in CA1 hippocampal area of aged rats is rescued by D-cycloserine. Eur J Neurosci 25:2260-2268.
13. Bisaz R, Sandi C (2012) Vulnerability of conditional NCAM-deficient mice to develop stress-induced behavioral alterations. Stress. Advance online publication. Retrieved Sept. 22, 2011. doi:10.3109/10253890.2011. 608226.
14. Bukalo O, Fentrop N, Lee AY, Salmen B, Law JW, Wotjak CT, Schweizer M, Dityatev A, Schachner M (2004) Conditional ablation of the neural cell adhesion molecule reduces precision of spatial learning, long-term potentiation, and depression in the CA1 subfield of mouse hippocampus. J Neurosci 24:1565-1577.
15. Chen G, Chen P, Tan H, Ma D, Dou F, Feng J, Yan Z (2008) Regulation of the NMDA receptor-mediated synaptic response by acetylcholinesterase inhibitors and its impairment in an animal model of Alzheimer's disease. Neurobiol Aging 29:1795-1804.
16. Ciocchi S, Herry C, Grenier F, Wolff SB, Letzkus JJ, Vlachos I, Ehrlich I, Sprengel R, Deisseroth K, Stadler MB, Müller C, Lüthi A (2010) Encoding of conditioned fear in central amygdala inhibitory circuits. Nature 468:277-282.
17. Clayton DA, Mesches MH, Alvarez E, Bickford PC, Browning MD (2002) A hippocampal NR2B deficit can mimic age-related changes in long-term potentiation and spatial learning in the Fischer 344 rat. J Neurosci 22:3628-3637.
18. Collingridge GL, Peineau S, Howland JG, Wang YT (2010) Long-term depression in the CNS. Nat Rev Neurosci 11:459-473.
19. Convit A, Wolf OT, de Leon MJ, Patalinjug M, Kandil E, Caraos C, Scherer A, Saint Louis LA, Cancro R (2001) Volumetric analysis of the pre-frontal regions: findings in aging and schizophrenia. Psychiatry Res 107:61-73.
20. Conzelman GM Jr, Jones RK (1956) On the physiologic disposition of cycloserine in experimental animals. Am Rev Tuberc 74:802-806.
21. Cox ET, Brennaman LH, Gable KL, Hamer RM, Glantz LA, Lamantia AS, Lieberman JA, Gilmore JH, Maness PF, Jarskog LF (2009) Developmental regulation of neural cell adhesion molecule in human prefrontal cortex. Neuroscience 162:96-105.
22. Cremer H, Lange R, Christoph A, Plomann M, Vopper G, Roes J, Brown R, Baldwin S, Kraemer P, Scheff S, Barthels D, Rajewsky K, Wille W (1994) Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 367:455-459.
23. Dityatev A, Dityateva G, Sytnyk V, Delling M, Toni N, Nikonenko I, Muller D, Schachner M (2004) Polysialylated neural cell adhesion molecule promotes remodeling and formation of hippocampal synapses. J Neurosci 24:9372-9382.
24. Dracheva S, Marras SA, Elhakem SL, Kramer FR, Davis KL, Haroutunian V (2001) N-methyl-D-aspartic acid receptor expression in the dorsolateral prefrontal cortex of elderly patients with schizophrenia. Am J Psychiatry 158:1400-1410.
25. Eckhardt M, Bukalo O, Chazal G, Wang L, Goridis C, Schachner M, Gerardy-Schahn R, Cremer H, Dityatev A (2000) Mice deficient in the polysialyltransferase ST8SiaIV/PST-1 allow discrimination of the roles of neural cell adhesion molecule protein and polysialic acid in neural development and synaptic plasticity. J Neurosci 20:5234-5244.
26. Evers MR, Salmen B, Bukalo O, Rollenhagen A, Bösl MR, Morellini F, Bartsch U, Dityatev A, Schachner M (2002) Impairment of L-type Ca2+ channel-dependent forms of hippocampal synaptic plasticity in mice deficient in the extracellular matrix glycoprotein tenascin-C. J Neurosci 22:7177-7194.
27. Florian C, Foltz J, Norreel JC, Rougon G, Roullet P (2006) Post-training intrahippocampal injection of synthetic poly-alpha-2,8-sialic acid-neural cell adhesion molecule mimetic peptide improves spatial long-term performance in mice. Learn Mem 13:335-341.
28. Fox CJ, Russell KI, Wang YT, Christie BR (2006) Contribution of NR2A and NR2B NMDA subunits to bidirectional synaptic plasticity in the hippocampus in vivo. Hippocampus 16:907-915.
29. Fox GB, Kennedy N, Regan CM (1995) Polysialylated neural cell adhesion molecule expression by neurons and astroglial processes in the rat dentate gyrus declines dramatically with increasing age. Int J Dev Neurosci 13:663-672.
30. Fux CM, Krug M, Dityatev A, Schuster T, Schachner M (2003) NCAM180 and glutamate receptor subtypes in potentiated spine synapses: an immunogold electron microscopic study. Mol Cell Neurosci 24:939-950.
31. Gao C, Gill MB, Tronson NC, Guedea AL, Guzmán YF, Huh KH, Corcoran KA, Swanson GT, Radulovic J (2010) Hippocampal NMDA receptor subunits differentially regulate fear memory formation and neuronal signal propagation. Hippocampus 20:1072-1082.
32. Gao XM, Sakai K, Roberts RC, Conley RR, Dean B, Tamminga CA (2000) Ionotropic glutamate receptors and expression of N-methyl-D-aspartate receptor subunits in subregions of human hippocampus: effects of schizophrenia. Am J Psychiatry 157:1141-1149.
33. Hammond MS, Sims C, Parameshwaran K, Suppiramaniam V, Schachner M, Dityatev A (2006) Neural cell adhesion molecule-associated polysialic acid inhibits NR2B-containing N-methyl-D-aspartate receptors and prevents glutamate-induced cell death. J Biol Chem 281:34859-34869.
34. 2+]i have to be reached to induce LTP and LTD in neocortical pyramidal cells. J Physiol Paris 90:317-319.
35. 2+ levels and the polarity of synaptic long-term modifications in rat visual cortex neurons. Eur J Neurosci 9:2309-2322.
36. Hood WF, Compton RP, Monahan JB (1989) D-cycloserine: a ligand for the N-methyl-D-aspartate coupled glycine receptor has partial agonist characteristics. Neurosci Lett 98:91-95.
37. 2+ channels in the induction of LTP. J Neurosci 13:568-576.
38. Huber KM, Mauk MD, Kelly PT (1995) Distinct LTP induction mechanisms: contribution of NMDA receptors and voltage-dependent calcium channels. J Neurophysiol 73:270-279.
39. Ibrahim HM, Hogg AJ Jr, Healy DJ, Haroutunian V, Davis KL, Meador- Woodruff JH (2000) Ionotropic glutamate receptor binding and subunit mRNA expression in thalamic nuclei in schizophrenia. Am J Psychiatry 157:1811-1823.
40. Javitt DC (2006) Is the glycine site half saturated or half unsaturated? Effects of glutamatergic drugs in schizophrenia patients. Curr Opin Psychiatry 19:151-157.
41. Kaur M, Sharma S, Kaur G (2008) Age-related impairments in neuronal plasticity markers and astrocytic GFAP and their reversal by late-onset short term dietary restriction. Biogerontology 9:441-454.
42. Kerr DS, Abraham WC (1995) Cooperative interactions among afferents govern the induction of homosynaptic long-term depression in the hippocampus. Proc Natl Acad Sci U S A 92:11637-11641.
43. Kirkpatrick B, Messias E, Harvey PD, Fernandez-Egea E, Bowie CR (2008) Is schizophrenia a syndrome of accelerated aging? Schizophr Bull 34:1024-1032.
44. Kiyama Y, Manabe T, Sakimura K, Kawakami F, Mori H, Mishina M (1998) Increased thresholds for long-term potentiation and contextual learning in mice lacking the NMDA-type glutamate receptor epsilon1 subunit. J Neurosci 18:6704-6712.
45. Kochlamazashvili G, Senkov O, Grebenyuk S, Robinson C, Xiao MF, Stummeyer K, Gerardy-Schahn R, Engel AK, Feig L, Semyanov A, Suppiramaniam V, Schachner M, Dityatev A (2010) Neural cell adhesion molecule-associated polysialic acid regulates synaptic plasticity and learning by restraining the signaling through GluN2B-containing NMDA receptors. J Neurosci 30:4171-4183.
46. Köhr G, Jensen V, Koester HJ, Mihaljevic AL, Utvik JK, Kvello A, Ottersen OP, Seeburg PH, Sprengel R, Hvalby O.(2003) Intracellular domains of NMDA receptor subtypes are determinants for long-term potentiation induction. J Neurosci 23:10791-10799.
47. Kutsuwada T, Kashiwabuchi N, Mori H, Sakimura K, Kushiya E, Araki K, Meguro H, Masaki H, Kumanishi T, Arakawa M, Mishina M (1992) Molecular diversity of the NMDA receptor channel. Nature 358:36-41.
48. Laxmi TR, Stork O, Pape HC (2003) Generalisation of conditioned fear and its behavioural expression in mice. Behav Brain Res 145:89-98.
49. Ledgerwood L, Richardson R, Cranney J (2004) D-cycloserine and the facilitation of extinction of conditioned fear: consequences for reinstatement. Behav Neurosci 118:505-513.
50. Levine ES, Crozier RA, Black IB, Plummer MR (1998) Brain-derived neurotrophic factor modulates hippocampal synaptic transmission by increasing N-methyl-D-aspartic acid receptor activity. Proc Natl Acad Sci U S A 95:10235-10239.
51. Li S, Tian X, Hartley DM, Feig LA (2006) Distinct roles for Ras-guanine nucleotide-releasing factor 1 (Ras-GRF1) and Ras-GRF2 in the induction of long-term potentiation and long-term depression. J Neurosci 26:1721-1729.
52. Li S, Jin M, Koeglsperger T, Shepardson NE, Shankar GM, Selkoe DJ (2011) Soluble A{beta} Oligomers Inhibit Long-Term Potentiation through a Mechanism Involving Excessive Activation of Extrasynaptic NR2BContaining NMDA Receptors. J Neurosci 31:6627-6638.
53. Lin SY, Wu K, Levine ES, Mount HT, Suen PC, Black IB (1998) BDNF acutely increases tyrosine phosphorylation of the NMDA receptor subunit 2B in cortical and hippocampal postsynaptic densities. Brain Res Mol Brain Res 55:20-27.
54. Liu L, Wong TP, Pozza MF, Lingenhoehl K, Wang Y, Sheng M, Auberson YP, Wang YT (2004) Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304:1021-1024.
55. Lynch MA (2004) Long-term potentiation and memory. Physiol Rev 84:87-136.
56. Malenka RC, Nicoll RA (1999) Long-term potentiation-a decade of progress? Science 285:1870-1874.
57. Maness PF, Schachner M (2007) Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat Neurosci 10:19-26.
58. Markram K, Gerardy-Schahn R, Sandi C (2007) Selective learning and memory impairments in mice deficient for polysialylated NCAM in adulthood. Neuroscience 144:788-796.
59. Massey PV, Johnson BE, Moult PR, Auberson YP, Brown MW, Molnar E, Collingridge GL, Bashir ZI (2004) Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. J Neurosci 24:7821-7828.
60. Mohr E, Knott V, Sampson M, Wesnes K, Herting R, Mendis T (1995) Cognitive and quantified electroencephalographic correlates of cycloserine treatment in Alzheimer's disease. Clin Neuropharmacol 18:28-38.
61. Morgan SL, Teyler TJ (2001) Electrical stimuli patterned after the thetarhythm induce multiple forms of LTP. J Neurophysiol 86:1289-1296.
62. Morris RG (1989) Synaptic plasticity and learning: selective impairment of learning rats and blockade of long-term potentiation in vivo by the N-methyl-D-aspartate receptor antagonist AP5. J Neurosci 9:3040-3057.
63. Morris RG, Anderson E, Lynch GS, Baudry M (1986) Selective impairment of learning and blockade of long-term potentiation by an N-methyl-Daspartate receptor antagonist, AP5. Nature 319:774-776.
64. Mothet JP, Rouaud E, Sinet PM, Potier B, Jouvenceau A, Dutar P, Videau C, Epelbaum J, Billard JM (2006) A critical role for the glial-derived neuromodulator D-serine in the age-related deficits of cellular mechanisms of learning and memory. Aging Cell 5:267-274.
65. Muller D, Wang C, Skibo G, Toni N, Cremer H, Calaora V, Rougon G, Kiss JZ (1996) PSA-NCAM is required for activity-induced synaptic plasticity. Neuron 17:413-422.
66. Muller D, Djebbara-Hannas Z, Jourdain P, Vutskits L, Durbec P, Rougon G, Kiss JZ (2000) Brain-derived neurotrophic factor restores long-term potentiation in polysialic acid-neural cell adhesion molecule-deficient hippocampus. Proc Natl Acad Sci U S A 97:4315-4320.
67. Murphy KJ, Regan CM (1999) Sequential training in separate paradigms impairs second task consolidation and learning-associated modulations of hippocampalNCAMpolysialylation. Neurobiol Learn Mem 72:28-38.
68. Murphy KJ, O'Connell AW, Regan CM (1996) Repetitive and transient increases in hippocampal neural cell adhesion molecule polysialylation state following multitrial spatial training. J Neurochem 67:1268-1274.
69. Newell KA, Zavitsanou K, Huang XF (2005) Ionotropic glutamate receptor binding in the posterior cingulate cortex in schizophrenia patients. Neuroreport 16:1363-1367.
70. Ni Dhú ill CM, Fox GB, Pittock SJ, O'Connell AW, Murphy KJ, Regan CM (1999) Polysialylated neural cell adhesion molecule expression in the dentate gyrus of the human hippocampal formation from infancy to old age. J Neurosci Res 55:99-106.
71. Norberg MM, Krystal JH, Tolin DF (2008) A meta-analysis of D-cycloserine and the facilitation of fear extinction and exposure therapy. Biol Psychiatry 63:1118-1126.
72. Onur OA, Schlaepfer TE, Kukolja J, Bauer A, Jeung H, Patin A, Otte DM, Shah NJ, Maier W, Kendrick KM, Fink GR, Hurlemann R (2010) The N-methyl-D-aspartate receptor co-agonist D-cycloserine facilitates declarative learning and hippocampal activity in humans. Biol Psychiatry 67:1205-1211.
73. Petralia RS, Sans N, Wang YX, Wenthold RJ (2005) Ontogeny of postsynaptic density proteins at glutamatergic synapses. Mol Cell Neurosci 29:436-452.
74. Potier B, Poindessous-Jazat F, Dutar P, Billard JM (2000) NMDA receptor activation in the aged rat hippocampus. Exp Gerontol 35:1185-1199.
75. Priestley T, Laughton P, Myers J, Le Bourdellés B, Kerby J, Whiting PJ (1995) Pharmacological properties of recombinant human N-methyl-Daspartate receptors comprising NR1a/NR2A and NR1a/NR2B subunit assemblies expressed in permanently transfected mouse fibroblast cells. Mol Pharmacol 48:841-848.
76. Quartermain D, Mower J, Rafferty MF, Herting RL, Lanthorn TH (1994) Acute but not chronic activation of the NMDA-coupled glycine receptor with D-cycloserine facilitates learning and retention. Eur J Pharmacol 257:7-12.
77. Richardson R, Ledgerwood L, Cranney J (2004) Facilitation of fear extinction by D-cycloserine: theoretical and clinical implications. Learn Mem 11:510-516.
78. Rodrigues SM, Schafe GE, LeDoux JE (2004) Molecular mechanisms underlying emotional learning and memory in the lateral amygdala. Neuron 44:75-91.
79. Rutishauser U (2008) Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat Rev Neurosci 9:26-35.
80. Sandi C, Merino JJ, Cordero MI, Kruyt ND, Murphy KJ, Regan CM (2003) Modulation of hippocampal NCAM polysialylation and spatial memory consolidation by fear conditioning. Biol Psychiatry 54:599-607.
81. Schuster T, Krug M, Hassan H, Schachner M (1998) Increase in proportion of hippocampal spine synapses expressing neural cell adhesion molecule NCAM180 following long-term potentiation. J Neurobiol 37:359-372.
82. Seki T (2002) Expression patterns of immature neuronal markers PSANCAM, CRMP-4 and NeuroD in the hippocampus of young adult and aged rodents. J Neurosci Res 70:327-334.
83. Seki T, Arai Y (1995) Age-related production of new granule cells in the adult dentate gyrus. Neuroreport 6:2479-2482.
84. Seki T, Arai Y (1999) Temporal and spacial relationships between PSANCAM- expressing, newly generated granule cells, and radial glia-like cells in the adult dentate gyrus. J Comp Neurol 410:503-513.
85. Senkov O, Sun M, Weinhold B, Gerardy-Schahn R, Schachner M, Dityatev A (2006) Polysialylated neural cell adhesion molecule is involved in induction of long-term potentiation and memory acquisition and consolidation in a fear-conditioning paradigm. J Neurosci 26:10888-109898.
86. Shankar S, Teyler TJ, Robbins N (1998) Aging differentially alters forms of long-term potentiation in rat hippocampal area CA1. J Neurophysiol 79:334-341.
87. Sheinin A, Shavit S, Benveniste M (2001) Subunit specificity and mechanism of action ofNMDApartial agonist D-cycloserine. Neuropharmacology 41:151-158.
88. Slack SE, Pezet S, McMahon SB, Thompson SW, Malcangio M (2004) Brain-derived neurotrophic factor induces NMDA receptor subunit one phosphorylation via ERK and PKC in the rat spinal cord. Eur J Neurosci 20:1769-1778.
89. Stork O, Welzl H, Wolfer D, Schuster T, Mantei N, Stork S, Hoyer D, Lipp H, Obata K, Schachner M (2000) Recovery of emotional behaviour in neural cell adhesion molecule (NCAM) null mutant mice through transgenic expression of NCAM180. Eur J Neurosci 12:3291-3306.
90. Stummeyer K, Dickmanns A, Mühlenhoff M, Gerardy-Schahn R, Ficner R (2005) Crystal structure of the polysialic acid-degrading endosialidase of bacteriophage K1F. Nat Struct Mol Biol 12:90-96.
91. Sytnyk V, Leshchyns'ka I, Nikonenko AG, Schachner M (2006) NCAMpromotes assembly and activity-dependent remodeling of the postsynaptic signaling complex. J Cell Biol 174:1071-1085.
92. Tang J, Wotjak CT, Wagner S, Williams G, Schachner M, Dityatev A (2001) Potentiated amygdaloid auditory-evoked potentials and freezing behavior after fear conditioning in mice. Brain Res 919:232-241.
93. Tang J, Wagner S, Schachner M, Dityatev A, Wotjak CT (2003) Potentiation of amygdaloid and hippocampal auditory-evoked potentials in a discriminatory fear-conditioning task in mice as a function of tone pattern and context. Eur J Neurosci 18:639-650.
94. Tereshchenko Y, Morellini F, Dityatev A, Schachner M, Irintchev A (2011) Neural cell adhesion molecule ablation in mice causes hippocampal dysplasia and loss of septal cholinergic neurons. J Comp Neurol 519:2475-2492.
95. Thompson LT, Disterhoft JF (1997) Age- and dose-dependent facilitation of associative eyeblink conditioning by D-cycloserine in rabbits. Behav Neurosci 111:1303-1312.
96. Tsai GE, Falk WE, Gunther J, Coyle JT (1999) Improved cognition in Alzheimer's disease with short-term D-cycloserine treatment. Am J Psychiatry 156:467-469.
97. Venero C, Herrero AI, Touyarot K, Cambon K, López-Fernández MA, Berezin V, Bock E, Sandi C (2006) Hippocampal up-regulation of NCAM expression and polysialylation plays a key role on spatial memory. Eur J Neurosci 23:1585-1595.
98. Williams EJ, Walsh FS, Doherty P (1994) The production of arachidonic acid can account for calcium channel activation in the second messenger pathway underlying neurite outgrowth stimulated by NCAM, N- cadherin, and L1. J Neurochem 62:1231-1234.
99. Wood GK, Tomasiewicz H, Rutishauser U, Magnuson T, Quirion R, Rochford J, Srivastava LK (1998) NCAM-180 knockout mice display increased lateral ventricle size and reduced prepulse inhibition of startle. Neuroreport 9:461-466.
100. Xu F, Plummer MR, Len GW, Nakazawa T, Yamamoto T, Black IB, Wu K (2006) Brain-derived neurotrophic factor rapidly increases NMDA receptor channel activity through Fyn-mediated phosphorylation. Brain Res 1121:22-34.
101. Yaka R, Biegon A, Grigoriadis N, Simeonidou C, Grigoriadis S, Alexandrovich AG, Matzner H, Schumann J, Trembovler V, Tsenter J, Shohami E (2007) D-cycloserine improves functional recovery and reinstates longterm potentiation (LTP) in a mouse model of closed head injury. FASEB J 21:2033-2041.
102. Yew DT, Li WP, Webb SE, Lai HW, Zhang L (1999) Neurotransmitters, peptides, and neural cell adhesion molecules in the cortices of normal elderly humans and Alzheimer patients: a comparison. Exp Gerontol 34:117-133.
103. Zlomuzica A, De Souza Silva MA, Huston JP, Dere E (2007) NMDA receptor modulation by D-cycloserine promotes episodic-like memory in mice. Psychopharmacology 193:503-509.