Caloric restriction and age affect synaptic proteins in hippocampal CA3 and spatial learning ability

Experimental Neurology

Volumn 211, Issue 1, 2008, Pages 141-149

  Adams, Michelle M ^a   Shi, Lei ^a   Linville, M Constance ^a   Forbes, M Elizabeth ^a   Long, Ashley B ^a   Bennett, Colleen ^a   Newton, Isabel G ^b   Carter, Christy S ^c   Sonntag, William E ^d   Riddle, David R ^a   Brunso Bechtold, Judy K ^a  

^a WAKE FOREST UNIVERSITY HEALTH SCIENCES   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

^d UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

Author keywords

AMPA; Dietary restriction; Morris water maze; NMDA; Rat; Synapses

Indexed keywords

AMPA RECEPTOR; GLUTAMATE RECEPTOR 1; GLUTAMATE RECEPTOR 2; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; NEUROTRANSMITTER; RECEPTOR SUBUNIT; SYNAPTOPHYSIN; TRACE ELEMENT;

AGING; ANIMAL EXPERIMENT; ARTICLE; CALORIC RESTRICTION; COGNITION; CONTROLLED STUDY; CORRELATION ANALYSIS; DIET RESTRICTION; HIPPOCAMPUS; LEARNING; LIFESPAN; MALE; MAZE TEST; MEMBRANE VESICLE; MEMORY; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; RELIABILITY; SPATIAL DISCRIMINATION; SYNAPSE; TASK PERFORMANCE;

AGE FACTORS; AGING; ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; CALORIC RESTRICTION; GENE EXPRESSION REGULATION; HIPPOCAMPUS; LEARNING; MALE; MAZE LEARNING; RATS; RECEPTORS, GLUTAMATE; SPACE PERCEPTION; SWIMMING;

EID: 42749087468     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2008.01.016     Document Type: Article

References (58)

1. Adams M.M., Smith T.D., Moga D., Gallagher M., Wang Y., Wolfe B.B., Rapp P.R., and Morrison J.H. 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 (2001) 230-243
2. Amaral D.G., and Witter M.P. Hippocampal formation. In: Paxinos G. (Ed). The Rat Nervous System (1995) 443-495
3. Brun V.H., Otnass M.K., Molden S., Steffenach H.A., Witter M.P., Moser M.B., and Moser E.I. Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 296 (2002) 2243-2246
4. Calhoun M.E., Kurth D., Phinney A.L., Long J.M., Hengemihle J., Mouton P.R., Ingram D.K., and Jucker M. Hippocampal neuron and synaptophysin-positive bouton number in aging C57BL/6 mice. Neurobiol. Aging 19 (1998) 599-606
5. Clark A.S., Magnusson K.R., and Cotman C.W. In vitro autoradiography of hippocampal excitatory amino acid binding in aged Fischer 344 rats: relationship to performance on the Morris water maze. Behav. Neurosci. 106 (1992) 324-335
6. Clayton D.A., and Browning M.D. Deficits in the expression of the NR2B subunit in the hippocampus of aged Fisher 344 rats. Neurobiol. Aging 22 (2001) 165-168
7. Clayton D.A., Mesches M.H., Alvarez E., Bickford P.C., and Browning M.D. A hippocampal NR2B deficit can mimic age-related changes in long-term potentiation and spatial learning in the Fischer 344 rat. J. Neurosci. 22 (2002) 3628-3637
8. Conrad C.D., Galea L.A., Kuroda Y., and McEwen B.S. Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behav. Neurosci. 110 (1996) 1321-1334
9. Eckles-Smith K., Clayton D., Bickford P., and Browning M.D. Caloric restriction prevents age-related deficits in LTP and in NMDA receptor expression. Brain Res. Mol. Brain Res. 78 (2000) 154-162
10. El Bakri N.K., Islam A., Zhu S., Elhassan A., Mohammed A., Winblad B., and Adem A. Effects of estrogen and progesterone treatment on rat hippocampal NMDA receptors: relationship to Morris water maze performance. J. Cell. Mol. Med. 8 (2004) 537-544
11. Gallagher M., Burwell R., and Burchinal M. Severity of spatial learning impairment in aging: development of a learning index for performance in the Morris water maze. Behav. Neurosci. 107 (1993) 618-626
12. Ganeshina O., Berry R.W., Petralia R.S., Nicholson D.A., and Geinisman Y. Differences in the expression of AMPA and NMDA receptors between axospinous perforated and nonperforated synapses are related to the configuration and size of postsynaptic densities. J. Comp. Neurol. 468 (2004) 86-95
13. Gazzaley A.H., Siegel S.J., Kordower J.H., Mufson E.J., and Morrison J.H. Circuit-specific alterations of N-methyl-D-aspartate receptor subunit 1 in the dentate gyrus of aged monkeys. Proc. Natl. Acad. Sci. USA 93 (1996) 3121-3125
14. Goodrick C.L., Ingram D.K., Reynolds M.A., Freeman J.R., and Cider N.L. Effects of intermittent feeding upon growth, activity, and lifespan in rats allowed voluntary exercise. Exp. Aging Res. 9 (1983) 203-209
15. Handelmann G.E., and Olton D.S. Spatial memory following damage to hippocampal CA3 pyramidal cells with kainic acid: impairment and recovery with preoperative training. Brain Res. 217 (1981) 41-58
16. Idrobo F., Nandy K., Mostofsky D.I., Blatt L., and Nandy L. Dietary restriction: effects on radial maze learning and lipofuscin pigment deposition in the hippocampus and frontal cortex. Arch. Gerontol. Geriatr. 6 (1987) 355-362
17. Ingram D.K., Weindruch R., Spangler E.L., Freeman J.R., and Walford R.L. Dietary restriction benefits learning and motor performance of aged mice. J. Gerontol. 42 (1987) 78-81
18. Jarrard L.E. Selective hippocampal lesions and behavior: effects of kainic acid lesions on performance of place and cue tasks. Behav. Neurosci. 97 (1983) 873-889
19. Jarrard L.E. Use of excitotoxins to lesion the hippocampus: update. Hippocampus 12 (2002) 405-414
20. Kullmann D.M., Asztely F., and Walker M.C. The role of mammalian ionotropic receptors in synaptic plasticity: LTP, LTD and epilepsy. Cell. Mol. Life Sci. 57 (2000) 1551-1561
21. Lisman J.E. Relating hippocampal circuitry to function: recall of memory sequences by reciprocal dentate-CA3 interactions. Neuron 22 (1999) 233-242
22. Luine V., Villegas M., Martinez C., and McEwen B.S. Repeated stress causes reversible impairments of spatial memory performance. Brain Res. 639 (1994) 167-170
23. Magarinos A.M., Verdugo J.M., and McEwen B.S. Chronic stress alters synaptic terminal structure in hippocampus. Proc. Natl. Acad. Sci. U. S. A 94 (1997) 14002-14008
24. Magnusson K.R. Aging of glutamate receptors: correlations between binding and spatial memory performance in mice. Mech. Ageing Dev. 104 (1998) 227-248
25. Magnusson K.R. 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 (2000) 1666-1674
26. Markowska A.L., and Savonenko A. Retardation of cognitive aging by life-long diet restriction: implications for genetic variance. Neurobiol. Aging 23 (2002) 75-86
27. Mayhew M., Renganathan M., and Delbono O. Effectiveness of caloric restriction in preventing age-related changes in rat skeletal muscle. Biochem. Biophys. Res. Commun. 251 (1998) 95-99
28. McEwen B.S., and Magarinos A.M. Stress and hippocampal plasticity: implications for the pathophysiology of affective disorders. Hum. Psychopharmacol. 16 (2001) S7-S19
29. McEwen B.S., de Leon M.J., Lupien S.J., and Meaney M.J. Corticosteroids, the aging brain and cognition. Trends Endocrinol. Metab. 10 (1999) 92-96
30. Monti B., Virgili M., and Contestabile A. Alterations of markers related to synaptic function in aging rat brain, in normal conditions or under conditions of long-term dietary manipulation. Neurochem. Int. 44 (2004) 579-584
31. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11 (1984) 47-60
32. Morris R.G., Garrud P., Rawlins J.N., and O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 297 (1982) 681-683
33. Morrison J.H., and Hof P.R. Life and death of neurons in the aging brain. Science 278 (1997) 412-419
34. Nakazawa K., Quirk M.C., Chitwood R.A., Watanabe M., Yeckel M.F., Sun L.D., Kato A., Carr C.A., Johnston D., Wilson M.A., and Tonegawa S. Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science 297 (2002) 211-218
35. Nakazawa K., Sun L.D., Quirk M.C., Rondi-Reig L., Wilson M.A., and Tonegawa S. Hippocampal CA3 NMDA receptors are crucial for memory acquisition of one-time experience. Neuron 38 (2003) 305-315
36. Newton I.G., Forbes M.E., Legault C., Johnson J.E., Brunso-Bechtold J.K., and Riddle D.R. Caloric restriction does not reverse aging-related changes in hippocampal BDNF. Neurobiol. Aging 26 (2005) 683-688
37. Newton, I.G., Forbes, M.E., Linville, M.C., Pang, H., Tucker, E.W., Riddle, D.R., Brunso-Bechtold, J.K., in press. Effects of aging and caloric restriction on dentate gyrus synapses and glutamate receptor subunits. Neurobiol. Aging. doi:10.1016/j.neurobiolaging.2007.03.009.
38. Nicolas A., Michaud M., Lavigne G., and Montplaisir J. The influence of sex, age and sleep/wake state on characteristics of periodic leg movements in restless legs syndrome patients. Clin. Neurophysiol. 110 (1999) 1168-1174
39. Pitsikas N., and Algeri S. Deterioration of spatial and nonspatial reference and working memory in aged rats: protective effect of life-long calorie restriction. Neurobiol. Aging 13 (1992) 369-373
40. Pitsikas N., Carli M., Fidecka S., and Algeri S. Effect of life-long hypocaloric diet on age-related changes in motor and cognitive behavior in a rat population. Neurobiol. Aging 11 (1990) 417-423
41. Poe B.H., Linville C., Riddle D.R., Sonntag W.E., and Brunso-Bechtold J.K. Effects of age and insulin-like growth factor-1 on neuron and synapse numbers in area CA3 of hippocampus. Neuroscience 107 (2001) 231-238
42. Ramsey M.M., Weiner J.L., Moore T.P., Carter C.S., and Sonntag W.E. Growth hormone treatment attenuates age-related changes in hippocampal short-term plasticity and spatial learning. Neuroscience 129 (2004) 119-127
43. Rapp P.R., and Gallagher M. Preserved neuron number in the hippocampus of aged rats with spatial learning deficits. Proc. Natl. Acad. Sci. U. S. A 93 (1996) 9926-9930
44. Rasmussen T., Schliemann T., Sorensen J.C., Zimmer J., and West M.J. Memory impaired aged rats: no loss of principal hippocampal and subicular neurons. Neurobiol. Aging 17 (1996) 143-147
45. Riedel G., Platt B., and Micheau J. Glutamate receptor function in learning and memory. Behav. Brain Res. 140 (2003) 1-47
46. Sandi C. [Glucocorticoid involvement in memory consolidation]. Rev. Neurol. 37 (2003) 843-848
47. Shapiro M.L., and Eichenbaum H. Hippocampus as a memory map: synaptic plasticity and memory encoding by hippocampal neurons. Hippocampus 9 (1999) 365-384
48. Shapiro M.L., Tanila H., and Eichenbaum H. Cues that hippocampal place cells encode: dynamic and hierarchical representation of local and distal stimuli. Hippocampus 7 (1997) 624-642
49. Shi L., Adams M.M., Linville M.C., Newton I.G., Forbes M.E., Long A.B., Riddle D.R., and Brunso-Bechtold J.K. Caloric restriction eliminates the aging-related decline in NMDA and AMPA receptor subunits in the rat hippocampus and induces homeostasis. Exp. Neurol. 206 (2007) 70-79
50. Shi L., Poe B.H., Constance L.M., Sonntag W.E., and Brunso-Bechtold J.K. Caloric restricted male rats demonstrate fewer synapses in layer 2 of sensorimotor cortex. Brain Res. 931 (2002) 32-40
51. Smith T.D., Adams M.M., Gallagher M., Morrison J.H., and Rapp P.R. Circuit-specific alterations in hippocampal synaptophysin immunoreactivity predict spatial learning impairment in aged rats. J. Neurosci. 20 (2000) 6587-6593
52. Sonntag W.E., Bennett S.A., Khan A.S., Thornton P.L., Xu X., Ingram R.L., and Brunso-Bechtold J.K. Age and insulin-like growth factor-1 modulate N-methyl-d-aspartate receptor subtype expression in rats. Brain Res. Bull. 51 (2000) 331-338
53. Sousa N., Lukoyanov N.V., Madeira M.D., Almeida O.F., and Paula-Barbosa M.M. Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience 97 (2000) 253-266
54. Stewart J., Mitchell J., and Kalant N. The effects of life-long food restriction on spatial memory in young and aged Fischer 344 rats measured in the eight-arm radial and the Morris water mazes. Neurobiol. Aging 10 (1989) 669-675
55. Stubley-Weatherly L., Harding J.W., and Wright J.W. Effects of discrete kainic acid-induced hippocampal lesions on spatial and contextual learning and memory in rats. Brain Res. 716 (1996) 29-38
56. Wenk G.L., and Barnes C.A. Regional changes in the hippocampal density of AMPA and NMDA receptors across the lifespan of the rat. Brain Res. 885 (2000) 1-5
57. West M.J., Slomianka L., and Gundersen H.J. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat. Rec. 231 (1991) 482-497
58. Woolley C.S., Gould E., Frankfurt M., and McEwen B.S. Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J. Neurosci. 10 (1990) 4035-4039