A Hippocampal NR2B Deficit Can Mimic Age-Related Changes in Long-Term Potentiation and Spatial Learning in the Fischer 344 Rat

Journal of Neuroscience

Volumn 22, Issue 9, 2002, Pages 3628-3637

  Clayton, Daniel A ^a   Mesches, Michael H ^a,b   Alvarez, Enriquez ^a   Bickford, Paula C ^b,c   Browning, Michael D ^a,d  

^a UNIVERSITY OF COLORADO   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c UNIVERSITY OF SOUTH FLORIDA   (United States)

^d University of South Florida ^*  (United States)

Author keywords

Aging; Antisense; Learning; LTP; NMDA; NR2B

Indexed keywords

ANTISENSE OLIGODEOXYNUCLEOTIDE; METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; PROTEIN SUBUNIT; RECEPTOR; UNCLASSIFIED DRUG; 7 CHLOROKYNURENIC ACID; 7-CHLOROKYNURENIC ACID; AMINO ACID RECEPTOR BLOCKING AGENT; ANTISENSE OLIGONUCLEOTIDE; CALCIUM CHANNEL BLOCKING AGENT; DRUG DERIVATIVE; KYNURENIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NR2B NMDA RECEPTOR; SPERMINE;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; CORRELATION ANALYSIS; HIPPOCAMPUS; LEARNING DISORDER; LONG TERM POTENTIATION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RAT STRAIN; ACTION POTENTIAL; ANIMAL; ANIMAL BEHAVIOR; CATHETERIZATION; DRUG EFFECT; ELECTROSTIMULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; FISCHER 344 RAT; GENE EXPRESSION; GENETICS; IN VITRO STUDY; MAZE TEST; METABOLISM; MICROINJECTION; PHYSIOLOGY; WESTERN BLOTTING;

ACTION POTENTIALS; AGING; ANIMALS; BEHAVIOR, ANIMAL; BLOTTING, WESTERN; CALCIUM CHANNEL BLOCKERS; CATHETERIZATION; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GENE EXPRESSION; HIPPOCAMPUS; KYNURENIC ACID; LONG-TERM POTENTIATION; MALE; MAZE LEARNING; MICROINJECTIONS; OLIGONUCLEOTIDES, ANTISENSE; RATS; RATS, INBRED F344; RECEPTORS, N-METHYL-D-ASPARTATE; SPERMINE;

EID: 0036583275     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-09-03628.2002     Document Type: Article

References (51)

1. Adams MM, Smith TD, Moga D, Gallagher M, Wang Y, Wolfe BB, Rapp PR, Morrison JH (2001) Hippocampal dependent learning ability correlates with N-methyl-D-aspartate (NMDA) receptor levels in CA3 neurons of young and aged rats. J Comp Neurol 432:230-243.
2. Audinat E, Lambolez B, Rossier J, Crepel F (1994) Activity-dependent regulation of N-methyl-D-aspartate receptor subunit expression in rat cerebellar granule cells. Eur J Neurosci 6:1792-1800.
3. Audinat E, Lambolez B, Rossier J (1996) Functional and molecular analysis of glutamate-gated channels by patch-clamp and RT-PCR at the single cell level. Neurochem Int 28:119-136.
4. Bach ME, Barad M, Son H, Zhuo M, Lu YF, Shih R, Mansuy I, Hawkins RD, Kandel ER (1999) Age-related defects in spatial memory are correlated with defects in the late phase of hippocampal long-term potentiation in vitro and are attenuated by drugs that enhance the cAMP signaling pathway. Proc Natl Acad Sci USA 96:5280-5285.
5. Backman C, Rose GM, Hoffer BJ, Henry MA, Bartus RT, Friden P, Granholm AC (1996) Systemic administration of a nerve growth factor conjugate reverses age-related cognitive dysfunction and prevents cholinergic neuron atrophy. J Neurosci 16:5437-5442.
6. Barnes CA (1979) Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J Comp Physiol Psychol 93:74-104.
7. Barnes CA, Nadel L, Honig WK (1980) Spatial memory deficit in senescent rats. Can J Psychol 34:29-39.
8. Barnes CA, Rao G, Shen J (1997) Age-related decrease in the N-methyl-D-aspartateR-mediated excitatory postsynaptic potential in hippocampal region CA1. Neurobiol Aging 18:445-452.
9. Brimecombe JC, Boeckman FA, Aizenman E (1997) Functional consequences of NR2 subunit composition in single recombinant N-methyl-D-aspartate receptors. Proc Natl Acad Sci USA 94:11019-11024.
10. Campbell LW, Hao SY, Thibault O, Blalock EM, Landfield PW (1996) Aging changes in voltage-gated calcium currents in hippocampal CA1 neurons. J Neurosci 16:6286-6295.
11. Cavus I, Teyler T (1996) Two forms of long-term potentiation in area CA1 activate different signal transduction cascades. J Neurophysiol 76:3038-3047.
12. Clayton DA, Browning MD (2001) Deficits in the expression of the NR2B subunit in the hippocampus of aged Fisher 344 rats. Neurobiol Aging 22:165-168.
13. Costenla AR, de Mendonca A, Ribeiro JA (1999) Adenosine modulates synaptic plasticity in hippocampal slices from aged rats. Brain Res 851:228-234.
14. deToledo-Morrell L, Geinisman Y, Morrell F (1988) Age-dependent alterations in hippocampal synaptic plasticity: relation to memory disorders. Neurobiol Aging 9:581-590.
15. Eckles-Smith K, Clayton D, Bickford P, Browning MD (2000) Caloric restriction prevents age-related deficits in LTP and in NMDA receptor expression. Brain Res Mol Brain Res 78:154-162.
16. Flint AC, Maisch US, Weishaupt JH, Kriegstein AR, Monyer H (1997) NR2A subunit expression shortens NMDA receptor synaptic currents in developing neocortex. J Neurosci 17:2469-2476.
17. Gallagher M, Burwell R, Burchinal M (1993) Severity of spatial learning impairment in aging: development of a learning index for performance in the Morris water maze. Behav Neurosci 107:618-626.
18. Gould TJ, Bickford PC (1997) Age-related deficits in the cerebellar beta adrenergic signal transduction cascade in Fischer 344 rats. J Pharmacol Exp Ther 281:965-971.
19. Granger R, Deadwyler S, Davis M, Moskovitz B, Kessler M, Rogers G, Lynch G (1996) Facilitation of glutamate receptors reverses an age-associated memory impairment in rats. Synapse 22:332-337.
20. 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.
21. Izumi Y, Zorumski CF (1998) LTP in CA1 of the adult rat hippocampus and voltage-activated calcium channels. NeuroReport 9:3689-3691.
22. Kuehl-Kovarik MC, Magnusson KR, Premkumar LS, Partin KM (2000) Electrophysiological analysis of NMDA receptor subunit changes in the aging mouse cortex. Mech Aging Dev 115:39-59.
23. Lanahan A, Lyford G, Stevenson GS, Worley PF, Barnes CA (1997) Selective alteration of long-term potentiation-induced transcriptional response in hippocampus of aged, memory-impaired rats. J Neurosci 17:2876-2885.
24. Landfield PW, Lynch G (1977) Impaired monosynaptic potentiation in in vitro hippocampal slices from aged, memory-deficient rats. J Gerontol 32:523-533.
25. Landfield PW, McGaugh JL, Lynch G (1978) Impaired synaptic potentiation processes in the hippocampus of aged, memory-deficient rats. Brain Res 150:85-101.
26. Lynch MA (1998) Age-related impairment in long-term potentiation in hippocampus: a role for the cytokine, interleukin-1 beta? Prog Neurobiol 56:571-589.
27. Magnusson KR (2000) Declines in mRNA expression of different subunits may account for differential effects of aging on agonist and antagonist binding to the NMDA receptor. J Neurosci 20:1666-1674.
28. Markowska AL, Mooney M, Sonntag WE (1998) Insulin-like growth factor-1 ameliorates age-related behavioral deficits. Neuroscience 87:559-569.
29. McGahon BM, Murray CA, Horrobin DF, Lynch MA (1999) Age-related changes in oxidative mechanisms and LTP are reversed by dietary manipulation. Neurobiol Aging 20:643-653.
30. Meguro H, Mori H, Araki K, Kushiya E, Kutsuwada T, Yamazaki M, Kumanishi T, Arakawa M, Sakimura K, Mishina M (1992) Functional characterization of a heteromeric NMDA receptor channel expressed from cloned cDNAs. Nature 357:70-74.
31. Moore CI, Browning MD, Rose GM (1993) Hippocampal plasticity induced by primed burst, but not long-term potentiation, stimulation is impaired in area CA1 of aged Fischer 344 rats. Hippocampus 3:57-66.
32. Morgan SL, Teyler TJ (1999) VDCCs and NMDARs underlie two forms of LTP in CA1 hippocampus in vivo. J Neurophysiol 82:736-740.
33. Myers SJ, Dingledine R, Borges K (1999) Genetic regulation of glutamate receptor ion channels. Annu Rev Pharmacol Toxicol 39:221-241.
34. Nayak A, Zastrow DJ, Lickteig R, Zahniser NR, Browning MD (1998) Maintenance of late-phase LTP is accompanied by PKA-dependent increase in AMPA receptor synthesis. Nature 394:680-683.
35. Rumbaugh G, Vicini S (1999) Distinct synaptic and extrasynaptic NMDA receptors in developing cerebellar granule neurons. J Neurosci 19:10603-10610.
36. 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.
37. Sonntag WE, Bennett SA, Khan AS, Thornton PL, Xu X, Ingram RL, Brunso-Bechtold JK (2000) Age and insulin-like growth factor-1 modulate N-methyl-D-aspartate receptor subtype expression in rats. Brain Res Bull 51:331-338.
38. Sprengel R, Suchanek B, Amico C, Brusa R, Burnashev N, Rozov A, Hvalby O, Jensen V, Paulsen O, Andersen P, Kim JJ, Thompson RF, Sun W, Webster LC, Grant SG, Eilers J, Konnerth A, Li J, McNamara JO, Seeburg PH (1998) Importance of the intracellular domain of NR2 subunits for NMDA receptor function in vivo. Cell 92:279-289.
39. Stocca G, Vicini S (1998) Increased contribution of NR2A subunit to synaptic NMDA receptors in developing rat cortical neurons. J Physiol (Lond) 507:13-24.
40. Tang YP, Shimizu E, Dube GR, Rampon C, Kerchner CA, Zhuo M, Liu G, Tsien JZ (1999) Genetic enhancement of learning and memory in mice. Nature 401:63-69.
41. Thibault O, Porter NM, Chen KC, Blalock EM, Kaminker PG, Clodfelter GV, Brewer LD, Landfield PW (1998) Calcium dysregulation in neuronal aging and Alzheimer's disease: history and new directions. Cell Calcium 24:417-433.
42. Tovar KR, Westbrook GL (1999) The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. J Neurosci 19:4180-4188.
43. Tovar KR, Sprouffske K, Westbrook GL (2000) Fast NMDA receptor-mediated synaptic currents in neurons from mice lacking the epsilon2 (NR2B) subunit. J Neurophysiol 83:616-620.
44. Vallano ML (1998) Developmental aspects of NMDA receptor function. Crit Rev Neurobiol 12:177-204.
45. Vallano ML, Lambolez B, Audinat E, Rossier J (1996) Neuronal activity differentially regulates NMDA receptor subunit expression in cerebellar granule cells. J Neurosci 16:631-639.
46. Ward MT, Oler JA, Markus EJ (1999a) Hippocampal dysfunction during aging I: deficits in memory consolidation. Neurobiol Aging 20:363-372.
47. Ward MT, Stoelzel CR, Markus EJ (1999b) Hippocampal dysfunction during aging II: deficits on the radial-arm maze. Neurobiol Aging 20:373-380.
48. Williams JH, Li YG, Nayak A, Errington ML, Murphy KP, Bliss TV (1993) The suppression of long-term potentiation in rat hippocampus by inhibitors of nitric oxide synthase is temperature and age dependent, Neuron 11:877-884.
49. Yau JL, Olsson T, Morris RG, Noble J, Seckl JR (1996) Decreased NGFI-A gene expression in the hippocampus of cognitively impaired aged rats. Brain Res Mol Brain Res 42:354-357.
50. Zhao HM, Wenthold RJ, Petralia RS (1998) Glutamate receptor targeting to synaptic populations on Purkinje cells is developmentally regulated. J Neurosci 18:5517-5528.
51. Zhong J, Carrozza DP, Williams K, Pritchett DB, Molinoff PB (1995) Expression of mRNAs encoding subunits of the NMDA receptor in developing rat brain. J Neurochem 64:531-539.