Functional integrity of NMDA-dependent LTP induction mechanisms across the lifespan of F-344 rats

Learning Memory

Volumn 3, Issue 2-3, 1996, Pages 124-137

  Barnes, Carol A ^a,b,c   Rao, Geeta ^c   McNaughton, Bruce L ^a,b,c  

^a University of Arizona   (United States)

^b UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; ELECTROSTIMULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; LEARNING; LONG TERM POTENTIATION; NONHUMAN; PRIORITY JOURNAL; RAT; SPATIAL MEMORY; SYNAPSE;

EID: 0029976891     PISSN: 10720502     EISSN: None     Source Type: Journal    
DOI: 10.1101/lm.3.2-3.124     Document Type: Article

References (101)

1. Albert, M.S. 1988. General issues in geriatric neuropsychology. In Geriatric neuropsychology (ed. M.S. Albert and M.B. Boss), pp. 3-10. Guilford Press, New York, NY.
2. Barnes, C.A. 1979. Memory deficits associated with senescence: A neurophysiological and behavioral study in the rat. J. Comp. Physiol. Psychol 931: 74-104.
3. _ 1990. Animal models of age-related cognitive decline. In Handbook of neuropsychology (ed. F. Boller and J. Grafman), pp. 169-196 Elsevier Science Publishers, Amsterdam, The Netherlands.
4. _ 1994 Normal aging: Regional specific changes in hippocampal synaptic transmission. Trends Neurosci. 17: 13-18.
5. _. 1995. Involvement of LTP in memory: Are we "searching under the street light?" Neuron 15: 751-754.
6. Barnes, C.A. and B.L. McNaughton. 1979. Neurophysiological comparison of dendritic cable properties in adolescent, middle-aged, and senescent rats. Exp. Brain Res. 5: 195-206.
7. _. 1980a. Physiological compensation for loss of afferent synapses in rat hippocampal granule cells during senescence. J. Physiol 309: 473-485.
8. _. 1980b. Spatial memory and hippocampal synaptic plasticity in middle-aged and senescent rats. In Psychobiology of aging: Problems and perspectives (ed D. Stein), pp. 253-272. Elsevier Press, New York, NY.
9. _. 1985. An age comparison of the rates of acquisition and forgetting of spatial information in relation to long-term enhancement of hippocampal synapses. Behav. Neurosci. 99: 1040-1048.
10. Barnes, C.A., G. Rao, and B.L. McNaughton. 1987. Increased electrotonic coupling in aged rat hippocampus: A possible mechanism for cellular excitability changes. J Comp Neurol. 259: 549-558.
11. Barnes, C.A., G. Rao, T.C. Foster, and B L. McNaughton. 1992. Region-specific age effects on AMPA sensitivity: Electrophysiological evidence for loss of synaptic contacts in hippocampal field CA1. Hippocampus 2: 457-468.
12. Barnes, C.A., A. Treves, G. Rao, and J. Shen. 1994. Electrophysiological markers of cognitive aging. Region specificity and computational consequences. Semin. Neurosci. 6: 359-367.
13. Baudry, M., D.S. Arst, and G. Lynch. 1981. Increased [3H] glutamate binding in aged rats. Brain Res 223: 195-198.
14. Bauman, L.A , C.D. Mahle, C.G Boissard, and V.K. Gribkoff. 1992. Age-dependence of effects of A1 adenosine receptor antagonism in rat hippocampal slices. J. Neurophysiol. 68: 629-638.
15. Baxter, M.G., T.H. Lanthorn, K.M. Frick, S. Golski, R.Q. Wan, and D.S. Olton. 1994. D-cycloserine, a novel cognitive enhancer, improves spatial memory in aged rats. Neurobiol. Aging 15: 207-213.
16. Bliss, T.V.P. and T. Lømo. 1973. Long-lasting potentiation of synaptic transmission in the dentate area of the unanaesthetised rabbit following stimulation of perforant path. J. Pbysiol. 232: 357-374.
17. Bonhaus, D., W. Perry, and J. McNamara. 1990. Decreased density, but not number, of N-methyl-D-aspartate, glycine and phencyclidine binding sites in hippocampus of senescent rats. Brain Res 532: 82-86.
18. Casoli, T., C. Spagna, P. Fattoretti, R. Gesuita, and C. Bertoni-Freddari. 1996. Neuronal plasticity in aging: A quantitative immunohistochemical study of GAP-43 distribution in discrete regions of the brain. Brain Res. 714: 111-117.
19. Castorina, M., A.M. Ambrosini, A. Giuliani, L. Pacifici, and L. Angelucci. 1993. A cluster analysis study of acetyl-L-carnitine effect on NMDA receptors in aging. Exp. Gerontol. 28: 537-548
20. Cimino, M., P. Mariani, S. Colombo, F. Cattebeni, and J. Meldolesi. 1993. [3H]-CGP 39653 mapping of glutamatergic N-methyl-D-aspartate in the brain of aged rats. Neurosci. Res. Commun. 12: 31-39.
21. Clark, A , K. Magnusson, and C. Cotman. 1992. Invitro autoradiography of hippocampal excitatory amino acid binding in aged Fischer 344 rats: Relationship to performance on the Morris water maze. Behav. Neurosci. 106: 324-335.
22. Cohen, N.J. and H. Eichenbaum. 1993. Memory, amnesia, and the hippocampal system. MIT Press, Cambridge, MA.
23. Cohen, S.A. and W.E. Muller. 1992. Age-related alterations of NMDA-receptor properties in the mouse forebrain: Partial restoration by chronic phosphatidylserine treatment. Brain Res. 584: 174-180.
24. Collingridge, G.L. 1987. Synaptic plasticity. The role of NMDA receptors in learning and memory. Nature 330: 604-605.
25. Collingridge, G.L., S.J. Kehl, and H. McLennan. 1983. The antagonism of amino acid-induced excitation of rat hippocampal CA1 neurons in vitro. J. Physiol. 334: 19-31.
26. Craik, F.I.M., N.D. Anderson, S.A. Kerr, and K.Z.H. Li. 1995. Memory changes in normal aging. In Handbook of memory disorders (ed. A.D. Baddeley, B.A. Wilson, and F.N. Watts), pp. 211-241. Wiley, New York, NY
27. Davis, S., A.L. Markowska, G.L. Wenk, and C.A. Barnes. 1993. Acetyl-L-carnitine: Behavioral, electrophysiological, and neurochemical effects. Neurobiol. Aging 14: 107-115.
28. de Toledo-Morrell, L., Y. Geinisman, and F. Morrell. 1988. Age-dependent alterations in hippocampal synaptic plasticity: Relation to memory disorders. Neurobiol. Aging 9: 581-590.
29. Deupree, D.L., D.A. Turner, and C.L. Watter. 1991. Spatial performance correlates with in vitro potentiation in young and aged Fischer 344 rats. Brain Res. 554: 1-9.
30. Deupree, D.L., J. Bradley, and D.A. Turner. 1993. Age-related alterations in potentiation in the CA1 region in F344 rats. Neurobiol. Aging 14: 249-258.
31. Fiore, L. and L. Rampello. 1989. L-acetylcarnitine attenuates the age-dependent decrease of NMDA-sensitive glutamate receptors in rat hippocampus. Acta Neurologica 11: 346-350.
32. Foster, T.C., C.A. Barnes, G. Rao, and B.L. McNaughton. 1991. Increase in perforant path quantal size in aged F-344 rats. Neurobiol. Aging 12: 441-448.
33. Gallagher, M., E. Bostock, and R. King. 1985. Effects of opiate antagonists on spatial memory in young and aged rats. Behav. Neural Biol. 44: 374-385.
34. Gallagher, M., R.D. Burwell, M.H. Kodsi, M. McKinney, S. Southerland, L. Vella-Rountree, and M.H. Lewis. 1990. Markers for biogenic amines in the aged rat brain: Relationship to decline in spatial learning ability. Neurobiol. Aging 11: 507-514.
35. Gallagher, M., R. Burwell, and M. Burchinal. 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.
36. Geinisman, Y., L. de Toledo-Morrell, and F. Morrell. 1986a. Aged rats need a preserved complement of perforated axospinous synapses per hippocampal neuron to maintain good spatial memory. Brain Res. 398: 266-275.
37. _. 1986b. Loss of perforated synapses in the dentate gyrus: Morphological substrate of memory deficit in aged rats. Proc Nat. Acad. Sci. 83: 3027-3031.
38. Geinisman, Y., L. de Toledo-Morrell, F. Morrell, I.S. Persina, and M. Rossi. 1992. Structural synaptic plasticity associated with the induction of long-term potentiation is preserved in the dentate gyrus of aged rats. Hippocampus 2: 445-456.
39. Geinisman, Y., L. de Toledo-Morrell, F. Morrell, and R.E. Heller. 1995. Hippocampal markers of age-related memory dysfunction: Behavioral, electrophysiological and morphological perspectives. Prog. Neurobiol. 45: 223-252.
40. Gribkoff, V K and L A. Bauman. 1992. Endogenous adenosine contributes to hypoxic synaptic depression in hippocampus from young and aged rats. J. Neurophysiol. 68: 620-628.
41. Gustafsson, B. and H. Wigström. 1986. Hippocampal long-lasting potentiation produced by pairing single volleys and brief conditioning tetani evoked in separate afferents. J. Neurosci 6: 1575-1582.
42. Gustafsson, B., W. Wigström, W. Abraham, and Y.-Y. Huang. 1987 Long-term potentiation in the hippocampus using depolarizing current pulses as the conditioning stimulus to single volley synaptic potentials. J. Neurosci. 7: 774-780.
43. Haas, H., B. Schaerer, and M. Vosmansky. 1979. A simple perfusion chamber for the study of nervous tissue slices in vitro. J. Neurosci. Methods 1: 323-325.
44. Hori, N., I. Hirotsu, P.J. Davis, and D.O. Carpenter. 1992. Long-term potentiation is lost in aged rats but preserved by calorie restriction. Neuroreport 3: 1085-1088.
45. Ingram, D.K., P Garofalo, E.L. Spangler, C.R. Mantione, I. Odano, and E.D. London. 1992. Reduced density of NMDA receptors and increased sensitivity to dizocilpine-induced learning impairment in aged rats. Brain Res. 580: 273-280.
46. Ingram, D.K., A. Shimada, A. Mukhin, and E.D. London. 1996. Evaluating the glutamate hypothesis of geriatric memory impairment: Focus on hippocampal NMDA receptors. Perspectives Brain Aging Res. 1: 30-35.
47. Kerr, D.S., L.W. Campbell, S.-Y. Hao, and P.W. Landfield. 1989. Corticosteroid modulation of hippocampal potentials: Increased effect with aging. Science 245: 1505-1509.
48. Kerr, D.S., L.W. Campbell, M.D. Applegate, A. Brodish, and P.W. Landfield. 1991. Chronic stress-induced acceleration of electrophysiologic and morphometric biomarkers of hippocampal aging. J. Neurosci. 11: 1316-1326.
49. Kito, S., R. Miyoshi, and T. Nomoto. 1990. Influence of age on NMDA receptor complex in rat brain studied by in vitro autoradiography. J. Histochem. Cytochem. 38: 1725-1731.
50. 3H]CGS 19755. Neurobiol. Aging 17: 453-457.
51. Landfield, P.W. 1988. Hippocampal neurobiological mechanisms of age-related memory dysfunction. Neurobiol Aging 9: 571-579.
52. Landfield, P.W. and G. Lynch. 1977. Impaired monosynaptic potentiation in in vitro hippocampal slices from aged, memory deficient rats. J Gerontol. 32: 523-533.
53. 2+-dependent afterhyperpolarizations in hippocampal neurons of aged rats. Science 226: 1089-1092
54. Landfield, P.W., G. Rose, L. Sandles, T.C. Wohlstadter, and G. Lynch. 1977. Patterns of astroglial hypertrophy and neuronal degeneration in the hippocampus of aged, memory-deficient rats. J. Gerontol. 32: 3-12.
55. Landfield, P.W., J.L. McGaugh, and G. Lynch. 1978 Impaired synaptic potentiation processes in the hippocampus of aged, memory-deficient rats. Brain Res. 150: 85-101.
56. 2+ ratios on frequency potentiation in hippocampal slices of young and aged rats. J. Neurophysiol 56: 797-811.
57. Lin, J.H., L.J. Way, and P.W. Gean. 1993. Pairing of pre-and postsynaptic activities in hippocampal CA1 neurons induces long-term modifications of NMDA receptor-mediated synaptic potential. Brain Res. 603: 117-120.
58. Lindner, M.D. and V.K. Gribkoff. 1992. Relationship between performance in the Morris water task, visual acuity, and thermoregulatory function in aged F-344 rats. Behav. Brain Res. 45: 45-55.
59. Lupica, C.R., W.R. Proctor, and T.V. Dunwiddie. 1992. Presynaptic inhibition of excitatory synaptic transmission by adenosine in rat hippocampus: Analysis of unitary EPSP variance measured by whole-cell recording. J. Neurosci. 12: 3753-3764.
60. Lynch, M.A. and K.L. Voss. 1994. Membrane arachidonic acid concentration correlates with age and induction of long-term potentiation in the dentate gyrus of the rat. Eur. J. Neurosci. 6: 1008-1014.
61. McNaughton, B L., R.M. Douglas, and G.V. Goddard. 1978. Synaptic enhancement in fascia dentata: Cooperativity among coactive afferents. Brain Res. 157: 277-293.
62. McNaughton, B.L., C.A. Barnes, and P. Anderson. 1981. Synaptic efficacy and EPSP summation in granule cells of rat fascia dentata studied in vitro J. Neurophysiol. 46: 952-966.
63. Magnusson, K.R. 1996. Glycine enhances binding to the NMDA receptor complex in aged mice, but does not correct the aging change. J Gerontol. 51A: B141-B147.
64. Magnusson, K.R. and C.W. Cotman. 1993. Effects of aging on NMDA and MK801 binding sites in mice. Brain Res. 604: 334-337.
65. Malenka, R.C. 1991. Postsynaptic factors control the duration of synaptic enhancement in area CA1 of the hippocampus. Neuron 6: 53-60
66. Meaney, M.J., D.H. Aitken, C. van Serkel, S. Bhatnagar, and R.M. Sapolsky. 1988. Effect of neonatal handling on age-related impairments associated with the hippocampus. Science 239: 766-768.
67. Moore, C.I , M.D. Browning, and G.M. Rose. 1993. Hippocampal plasticity induced by primed burst, but not long-term potentiation, stimulation is impaired in area CA1 of aged Fischer 334 rats. Hippocampus 3: 57-66.
68. Mover, J.R., Jr., L.T. Thompson, J.P. Black, and J.F. Disterhoft. 1992. Nimodipine increases excitability of rabbit CA1 pyramidal neurons in an age-and concentration-dependent manner. J. Neurophysiol. 68: 2100-2109.
69. Müller, W.E., S. Stoll, K. Scheuer, and A. Meichelböck. 1994. The function of the NMDA-receptor during normal brain aging. J. Neural Transmission 44: 145-158.
70. Ogawa, N., K. Mizukawa, K.M. Haba, M. Asanuma, and A. Mori. 1992. Effects of chronic bifemelane hydrochloride administration on receptors for N-methyl-D-aspartate in the aged rat brain. Neurochem. Res. 17: 687-691.
71. O'Keefe, J. and L Nadel. 1978. The hippocampus as a cognitive map Clarendon Press, Oxford, UK.
72. Papatheodoropoulos, C. and G. Kostopoulos. 1996. Age-related changes in excitability and recurrent inhibition in the rat CA1 hippocampal region. Eur J. Neurosci. 8: 510-520.
73. Pelleymounter, M.A., G. Beatty, and M. Gallagher. 1990. Hippocampal 3H-CPP binding and spatial learning deficits in aged rats. Psychobiology 18: 298-304.
74. Petersen, R.C. 1995. Normal aging, mild cognitive impairment, and early Alzheimer's disease. The Neurologist 1: 326-344.
75. Pittaluga, A., E. Fedele, C. Risiglione, and M. Raiteri. 1993. Age-related decreases of the NMDA receptor-mediated noradrenaline release in rat hippocampus and partial restoration by D-cycloserine. Eur. J. Pharmacol. 231: 129-134.
76. Potier, B., O. Rascol, F. Jazat, Y. Lamour, and P. Dutar. 1992. Alterations in the properties of hippocampal pyramidal neurons in the aged rat. Neuroscience 48: 793-806.
77. Potier, B., Y. Lamour, and P. Dutar. 1993. Age-related alterations in the properties of hippocampal pyramidal neurons among rat strains. Neurobiol. Aging 14: 17-25.
78. Rao, G., C.A. Barnes, B.L. McNaughton, J. Shen, and T.W. Abel. 1993. Age-related decrease in the NMDA-mediated EPSP in CA1. Soc. Neurosci. Abstr. 19: 794.
79. Rao, G., J. Shen, C A. Barnes, and B.L. McNaughton. 1995. Preserved LTP induction in CA1 of aged F-344 rats. Soc Neurosci. Abstr. 21: 940.
80. Rao, G., G.D. Stevenson, C.A. Barnes, B.L. McNaughton, and K.L. Weaver. 1996. Age-related decrease in the Schaffer collateral evoked EPSP in chronically implanted F-344 rats. Soc. Neurosci. Abstr 22: (in press)
81. Rapp, P.R. and D.G. Amaral. 1992. Individual differences in the cognitive and neurobiological consequences of normal aging. Trends Neurosci. 15: 340-345.
82. Reynolds, J.N. and P.L. Carlen. 1989. Diminished calcium currents in aged hippocampal dentate gyrus granule neurones. Brain Res. 479: 384-390.
83. Scheff, S.W., K.J. Anderson, and S.T. DeKosky. 1985 Strain comparison of synaptic density in hippocampal CA1 of aged rats. Neurobiol. Aging 6: 29-34.
84. Scheuer, K., S. Stoll, U. Paschke, R. Weiget, and W.E. Müller. 1995. N-methyl-D-aspartate receptor density and membrane fluidity as possible determinants of the decline of passive avoidance performance in aging. Pharmacol. Biochem. Behav. 50: 65-70.
85. Segal, M. 1982. Changes in neurotransmitter actions in the aged rat hippocampus. Neurobiol. Aging 3: 121-124.
86. Shahi, K. and M. Baudry. 1993. Glycine-induced changes in synaptic efficacy in hippocampal slices involve changes in AMPA receptors. Brain Res 627: 261-266.
87. Shen, J. and C.A. Barnes. 1996. Age-related decrease in cholinergic synaptic transmission in three hippocampal subfields. Neurobiol. Aging 17: 439-451.
88. Shimada, A., A. Mukhin, D.K. Ingram, and E.D. London. 1996. N-methyl-D-aspartate receptor binding in brains of rats at different ages. Neurobiol. Aging (in press).
89. Squire, L.R. 1992. Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 99: 195-231.
90. Stone, T.W. 1994. Excitatory amino acids and dementia. In Anti-dementia agents (ed. C.D. Nicholson), pp. 229-249. Academic Press, New York, NY.
91. Straube, K.T., R.A. Deyo, J.R. Moyer, Jr., and J.F. Disterhoft. 1990. Dietary nimodipine improves associative learning in aging rabbits Neurobiol. Aging 11: 659-661.
92. Tamaru, M., Y. Yoneda, K. Ogita, J. Shimizu, and Y. Nagata. 1991. Age-related decreases of the N-methyl-D-aspartate receptor complex in the rat cerebral cortex and hippocampus. Brain Res. 542: 83-90.
93. Taytor, L. and W.H. Griffith. 1993. Age-related decline in cholinergic synaptic transmission in hippocampus. Neurobiol. Aging 14: 509-515.
94. Thibault, O. and P.W. Landfield. 1996. Increase in single L-type calcium channels in hippocampal neurons during aging. Science 272: 1017-1020.
95. Tielen, A.M., W.J. Mollevanger, F.H. Lopes da Silva, and C.F. Hollander. 1983. Neuronal plasticity in hippocampal slices of extremely old rats. In Aging of the brain (ed. W.H. Gispen and J Traber), pp. 73-84. Elsevier Science Publishers, New York, NY.
96. Turner, D.A. and D.L. Deupree. 1991. Functional elongation of CA1 hippocampal neurons with aging in Fischer 344 rats. Neurobiol. Aging 12: 201-210.
97. Wenk, G.L., L.C. Walker, D.L. Price, and L.C. Cork. 1991. Loss of NMDA, but not GABA-A, binding in the brains of aged rats and monkeys. Neurobiol. Aging 12: 93-98.
98. Wigström, H., B. Gustafsson, Y.-Y. Huang, and W.C. Abraham. 1986. Hippocampal long-term potentiation is induced by pairing single afferent volleys with intracellularly injected depolarizing current pulses. Acta Physiol Scand. 126: 317-319.
99. Worley, P.F., R.V Bhat, J.M. Baraban, C.A. Erickson, B.L. McNaughton, and C.A. Barnes. 1993. Thresholds for synaptic activation of transciption factors in hippocampus: Correlation with long-term enhancement. J. Neurosci. 13: 4776-4786.
100. Yoshioka, N. and M. Sakurai. 1995. Postsynaptic depolarization in induction of long-term potentiation in the CA1 hippocampus. Neuroreport 6: 333-336.
101. Zyzak, D.R., T. Otto, H. Eichenbaum, and M. Gallagher. 1995. Cognitive decline associated with normal aging in rats: A neuropsychological approach. Learn. & Mem. 2: 1-16.