Age-induced alterations in hippocampal function and metabolism

Aging and Disease

Volumn 2, Issue 3, 2011, Pages 196-218

  Shetty, Pavan K ^a   Galeffi, Francesca ^a   Turner, Dennis A ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Aging; Caloric restriction; Ischemia; LTP; Mitochondrial dysfunction; NADH; ROS

Indexed keywords

EID: 84857706184     PISSN: None     EISSN: 21525250     Source Type: Journal    
DOI: None     Document Type: Review

References (198)

1. Mattson MP, Magnus T (2006). Ageing and neuronal vulnerability. Nat Rev Neurosci, 7: 278-94.
2. Rosenzweig ES, Barnes CA (2003). Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Prog Neurobiol, 69: 143-79.
3. Barnes CA (1979). Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J Comp Physiol Psychol, 93: 74-104.
4. Lynch MA, Voss KL (1994). Membrane arachidonic acid concentration correlates with age and induction of long-term potentiation in the dentate gyrus in the rat. Eur J Neurosci, 6: 1008-14.
5. McGahon B, Clements MP, Lynch MA (1997). The ability of aged rats to sustain long-term potentiation is restored when the age-related decrease in membrane arachidonic acid concentration is reversed. Neuroscience, 81: 9-16.
6. Shetty AK (2010). Reelin Signaling, Hippocampal Neurogenesis, and Efficacy of Aspirin Intake & Stem Cell Transplantation in Aging and Alzheimer's disease. Aging Dis, 1: 2-11.
7. Bishop NA, Lu T, Yankner BA (2010). Neural mechanisms of ageing and cognitive decline. Nature, 464: 529-35.
8. Banerjee R, Starkov AA, Beal MF, Thomas B (2009). Mitochondrial dysfunction in the limelight of Parkinson's disease pathogenesis. Biochim Biophys Acta, 1792: 651-63.
9. 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.
10. Turner DA, Adamson DC (2011). Neuronal-astrocyte metabolic interactions: understanding the transition into abnormal astrocytoma metabolism. J Neuropathol Exp Neurol, 70: 167-76.
11. Zarchin N, Meilin S, Rifkind J, Mayevsky A (2002). Effect of aging on brain energy-metabolism. Comp Biochem Physiol A Mol Integr Physiol, 132: 117-20.
12. Zhang X, Liu H, Wu J, Liu M, Wang Y (2009). Metabonomic alterations in hippocampus, temporal and prefrontal cortex with age in rats. Neurochem Int, 54: 481-7.
13. Rosenzweig ES, Rao G, McNaughton BL, Barnes CA (1997). Role of temporal summation in age-related long-term potentiation-induction deficits. Hippocampus, 7: 549-58.
14. Ames BN, Shigenaga MK, Hagen TM (1995). Mitochondrial decay in aging. Biochim Biophys Acta, 1271: 165-70.
15. Disterhoft JF, Moyer JR, Jr., Thompson LT (1994). The calcium rationale in aging and Alzheimer's disease. Evidence from an animal model of normal aging. Ann N Y Acad Sci, 747: 382-406.
16. Harman D (1956). Aging: a theory based on free radical and radiation chemistry. J Gerontol, 11: 298-300.
17. Jin K (2010). Modern Biological Theories of Aging. Aging Dis, 1: 72-74.
18. 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: 417-33.
19. Boveris A, Navarro A (2008). Brain mitochondrial dysfunction in aging. IUBMB Life, 60: 308-14.
20. Raffaello A, Rizzuto R (2011). Mitochondrial longevity pathways. Biochim Biophys Acta, 1813: 260-8.
21. Petit-Taboue MC, Landeau B, Desson JF, Desgranges B, Baron JC (1998). Effects of healthy aging on the regional cerebral metabolic rate of glucose assessed with statistical parametric mapping. Neuroimage, 7: 176-84.
22. Leenders KL, Perani D, Lammertsma AA, Heather JD, Buckingham P, Healy MJ, Gibbs JM, Wise RJ, Hatazawa J, Herold S, et al. (1990). Cerebral blood flow, blood volume and oxygen utilization. Normal values and effect of age. Brain, 113 (Pt 1): 27-47.
23. Hoyer S, Krier C (1986). Ischemia and aging brain. Studies on glucose and energy metabolism in rat cerebral cortex. Neurobiol Aging, 7: 23-9.
24. Gold PE (2005). Glucose and age-related changes in memory. Neurobiol Aging, 26 Suppl 1: 60-4.
25. McNay EC, Fries TM, Gold PE (2000). Decreases in rat extracellular hippocampal glucose concentration associated with cognitive demand during a spatial task. Proc Natl Acad Sci U S A, 97: 2881-5.
26. Foster KA, Margraf RR, Turner DA (2008). NADH hyperoxidation correlates with enhanced susceptibility of aged rats to hypoxia. Neurobiol Aging, 29: 598-613.
27. Roberts EL, Jr., Chih CP (1995). Age-related alterations in energy metabolism contribute to the increased vulnerability of the aging brain to anoxic damage. Brain Res, 678: 83-90.
28. Yager JY, Thornhill JA (1997). The effect of age on susceptibility to hypoxic-ischemic brain damage. Neurosci Biobehav Rev, 21: 167-74.
29. Malaguarnera M, Cammalleri L, Gargante MP, Vacante M, Colonna V, Motta M (2007). L-Carnitine treatment reduces severity of physical and mental fatigue and increases cognitive functions in centenarians: a randomized and controlled clinical trial. Am J Clin Nutr, 86: 1738-44.
30. Du H, Guo L, Yan S, Sosunov AA, McKhann GM, Yan SS (2010). Early deficits in synaptic mitochondria in an Alzheimer's disease mouse model. Proc Natl Acad Sci U S A, 107: 18670-5.
31. Santos RX, Correia SC, Wang X, Perry G, Smith MA, Moreira PI, Zhu X (2010). Alzheimer's disease: diverse aspects of mitochondrial malfunctioning. Int J Clin Exp Pathol, 3: 570-81.
32. Aliev G, Liu J, Shenk JC, Fischbach K, Pacheco GJ, Chen SG, Obrenovich ME, Ward WF, Richardson AG, Smith MA, Gasimov E, Perry G, Ames BN (2009). Neuronal mitochondrial amelioration by feeding acetyl-L-carnitine and lipoic acid to aged rats. J Cell Mol Med, 13: 320-333.
33. Navarro A, Lopez-Cepero JM, Bandez MJ, Sanchez-Pino MJ, Gomez C, Cadenas E, Boveris A (2008). Hippocampal mitochondrial dysfunction in rat aging. Am J Physiol Regul Integr Comp Physiol, 294: R501-9.
34. Kilbride SM, Telford JE, Davey GP (2008). Age-related changes in H2O2 production and bioenergetics in rat brain synaptosomes. Biochim Biophys Acta, 1777: 783-8.
35. Navarro A, Boveris A (2004). Rat brain and liver mitochondria develop oxidative stress and lose enzymatic activities on aging. Am J Physiol Regul Integr Comp Physiol, 287: R1244-9.
36. Navarro A, Sanchez Del Pino MJ, Gomez C, Peralta JL, Boveris A (2002). Behavioral dysfunction, brain oxidative stress, and impaired mitochondrial electron transfer in aging mice. Am J Physiol Regul Integr Comp Physiol, 282: R985-92.
37. Petrosillo G, Matera M, Casanova G, Ruggiero FM, Paradies G (2008). Mitochondrial dysfunction in rat brain with aging Involvement of complex I, reactive oxygen species and cardiolipin. Neurochem Int, 53: 126-31.
38. Ferrandiz ML, Martinez M, De Juan E, Diez A, Bustos G, Miquel J (1994). Impairment of mitochondrial oxidative phosphorylation in the brain of aged mice. Brain Res, 644: 335-8.
39. Xu K, Puchowicz MA, Sun X, LaManna JC (2010). Decreased brainstem function following cardiac arrest and resuscitation in aged rat. Brain Res, 1328: 181-9.
40. Harmon HJ, Nank S, Floyd RA (1987). Age-dependent changes in rat brain mitochondria of synaptic and non-synaptic origins. Mech Ageing Dev, 38: 167-177.
41. Manczak M, Jung Y, Park BS, Partovi D, Reddy PH (2005). Time-course of mitochondrial gene expressions in mice brains: implications for mitochondrial dysfunction, oxidative damage, and cytochrome c in aging. J Neurochem, 92: 494-504.
42. Jones TT, Brewer GJ (2010). Age-related deficiencies in complex I endogenous substrate availability and reserve capacity of complex IV in cortical neuron electron transport. Biochim Biophys Acta, 1797: 167-76.
43. Navarro A, Bandez MJ, Lopez-Cepero JM, Gomez C, Boveris A (2011). High doses of vitamin E improve mitochondrial dysfunction in rat hippocampus and frontal cortex upon aging. Am J Physiol Regul Integr Comp Physiol, 300: R827-34.
44. Larsson NG (2010). Somatic mitochondrial DNA mutations in mammalian aging. Annu Rev Biochem, 79: 683-706.
45. Reeve AK, Krishnan KJ, Turnbull D (2008). Mitochondrial DNA mutations in disease, aging, and neurodegeneration. Ann N Y Acad Sci, 1147: 21-9.
46. Rossignol R, Faustin B, Rocher C, Malgat M, Mazat JP, Letellier T (2003). Mitochondrial threshold effects. Biochem J, 370: 751-62.
47. Bender A, Krishnan KJ, Morris CM, Taylor GA, Reeve AK, Perry RH, Jaros E, Hersheson JS, Betts J, Klopstock T, Taylor RW, Turnbull DM (2006). High levels of mitochondrial DNA deletions in substantia nigra neurons in aging and Parkinson disease. Nat Genet, 38: 515-517.
48. Kraytsberg Y, Kudryavtseva E, McKee AC, Geula C, Kowall NW, Khrapko K (2006). Mitochondrial DNA deletions are abundant and cause functional impairment in aged human substantia nigra neurons. Nat Genet, 38: 518-20.
49. Fearnley JM, Lees AJ (1991). Agein and Parkinson's Disease: Substantia Nigra Regional Selectivity. Brain, 114: 2283-2301.
50. Stuart JA, Bourque BM, de Souza-Pinto NC, Bohr VA (2005). No evidence of mitochondrial respiratory dysfunction in OGG1-null mice deficient in removal of 8-oxodeoxyguanine from mitochondrial DNA. Free Radic Biol Med, 38: 737-45.
51. Balaban RS, Nemoto S, Finkel T (2005). Mitochondria, oxidants, and aging. Cell, 120: 483-95.
52. Brand MD (2010). The sites and topology of mitochondrial superoxide production. Exp Gerontol, 45: 466-72.
53. Xu J-X (2004). Radical Metabolism Is Partner to Energy Metabolism in Mitochondria. Ann N Y Acad Sci, 1011: 57-60.
54. Hamilton ML, Van Remmen H, Drake JA, Yang H, Guo ZM, Kewitt K, Walter CA, Richardson A (2001). Does oxidative damage to DNA increase with age? Proc Natl Acad Sci U S A, 98: 10469-74.
55. Mecocci P, MacGarvey U, Kaufman AE, Koontz D, Shoffner JM, Wallace DC, Beal MF (1993). Oxidative damage to mitochondrial DNA shows marked age-dependent increases in human brain. Ann Neurol, 34: 609-16.
56. Sanz A, Caro P, Ibanez J, Gomez J, Gredilla R, Barja G (2005). Dietary restriction at old age lowers mitochondrial oxygen radical production and leak at complex I and oxidative DNA damage in rat brain. J Bioenerg Biomembr, 37: 83-90.
57. Perez VI, Bokov A, Van Remmen H, Mele J, Ran Q, Ikeno Y, Richardson A (2009). Is the oxidative stress theory of aging dead? Biochim Biophys Acta, 1790: 1005-14.
58. Zhang Y, Ikeno Y, Qi W, Chaudhuri A, Li Y, Bokov A, Thorpe SR, Baynes JW, Epstein C, Richardson A, Van Remmen H (2009). Mice deficient in both Mn superoxide dismutase and glutathione peroxidase-1 have increased oxidative damage and a greater incidence of pathology but no reduction in longevity. J Gerontol A Biol Sci Med Sci, 64: 1212-20.
59. Perez VI, Van Remmen H, Bokov A, Epstein CJ, Vijg J, Richardson A (2009). The overexpression of major antioxidant enzymes does not extend the lifespan of mice. Aging Cell, 8: 73-5.
60. Schriner SE, Linford NJ, Martin GM, Treuting P, Ogburn CE, Emond M, Coskun PE, Ladiges W, Wolf N, Van Remmen H, Wallace DC, Rabinovitch PS (2005). Extension of murine life span by overexpression of catalase targeted to mitochondria. Science, 308: 1909-11.
61. Bodhinathan K, Kumar A, Foster TC (2010). Intracellular redox state alters NMDA receptor response during aging through Ca2+/calmodulin-dependent protein kinase II. J Neurosci, 30: 1914-24.
62. Disterhoft JF, Thompson LT, Moyer JR, Jr., Mogul DJ (1996). Calcium-dependent afterhyperpolarization and learning in young and aging hippocampus. Life Sci, 59: 413-20.
63. Landfield PW, Pitler TA (1984). Prolonged Ca2+-dependent afterhyperpolarizations in hippocampal neurons of aged rats. Science, 226: 1089-92.
64. Toescu EC, Verkhratsky A (2003). Neuronal ageing from an intraneuronal perspective: roles of endoplasmic reticulum and mitochondria. Cell Calcium, 34: 311-23.
65. Verkhratsky A, Toescu EC (1998). Calcium and neuronal ageing. Trends Neurosci, 21: 2-7.
66. Thibault O, Gant JC, Landfield PW (2007). Expansion of the calcium hypothesis of brain aging and Alzheimer's disease: minding the store. Aging Cell, 6: 307-17.
67. Popa-Wagner A, Buga AM, Kokaia Z (2011). Perturbed cellular response to brain injury during aging. Ageing Res Rev, 10: 71-9.
68. Barnett H (2002). Stroke prevention in the elderly. Clin Exp Hypertens, 24: 563.
69. Van Kooten F, Koudstaal PJ (1998). Epidemiology of post-stroke dementia. Haemostasis, 28: 124-33.
70. Farkas E, Luiten PG (2001). Cerebral microvascular pathology in aging and Alzheimer's disease. Prog Neurobiol, 64: 575-611.
71. Park L, Anrather J, Girouard H, Zhou P, Iadecola C (2007). Nox2-derived reactive oxygen species mediate neurovascular dysregulation in the aging mouse brain. J Cereb Blood Flow Metab, 27: 1908-18.
72. Floyd RA, Carney JM (1991). Age influence on oxidative events during brain ischemia/reperfusion. Arch Gerontol Geriatr, 12: 155-77.
73. Roberts EL, Jr., Rosenthal M, Sick TJ (1990). Age-related modifications of potassium homeostasis and synaptic transmission during and after anoxia in rat hippocampal slices. Brain Res, 514: 111-8.
74. Benzi G, Pastoris O, Marzatico F, Villa RF, Dagani F, Curti D (1992). The mitochondrial electron transfer alteration as a factor involved in the brain aging. Neurobiol Aging, 13: 361-8.
75. Martin RL, Lloyd HG, Cowan AI (1994). The early events of oxygen and glucose deprivation: setting the scene for neuronal death? Trends Neurosci, 17: 251-7.
76. Lipton P (1999). Ischemic cell death in brain neurons. Physiol Rev, 79: 1431-568.
77. Halestrap AP (2010). A pore way to die: the role of mitochondria in reperfusion injury and cardioprotection. Biochem Soc Trans, 38: 841-60.
78. Scarlett JL, Murphy MP (1997). Release of apoptogenic proteins from the mitochondrial intermembrane space during the mitochondrial permeability transition. FEBS Lett, 418: 282-6.
79. Sato E, Inoue A, Kurokawa T, Ishibashi S (1994). Early changes in glucose metabolism in the cerebrum of senescence accelerated mouse: involvement of glucose transporter. Brain Res, 637: 133-8.
80. Benzi G, Pastoris O, Villa RF, Giuffrida AM (1984). Effect of aging on cerebral cortex energy metabolism in hypoglycemia and posthypoglycemic recovery. Neurobiology of Aging, 5: 205-212.
81. Funahashi T, Floyd RA, Carney JM (1994). Age effect on brain pH during ischemia/reperfusion and pH influence on peroxidation. Neurobiol Aging, 15: 161-7.
82. Foster KA, Beaver CJ, Turner DA (2005). Interaction between tissue oxygen tension and NADH imaging during synaptic stimulation and hypoxia in rat hippocampal slices. Neuroscience, 132: 645-57.
83. Sims NR, Muyderman H (2010). Mitochondria, oxidative metabolism and cell death in stroke. Biochim Biophys Acta, 1802: 80-91.
84. Sims NR, Pulsinelli WA (1987). Altered mitochondrial respiration in selectively vulnerable brain subregions following transient forebrain ischemia in the rat. J Neurochem, 49: 1367-74.
85. Soane L, Kahraman S, Kristian T, Fiskum G (2007). Mechanisms of impaired mitochondrial energy metabolism in acute and chronic neurodegenerative disorders. J Neurosci Res, 85: 3407-15.
86. Toman J, Fiskum G (2011). Influence of aging on membrane permeability transition in brain mitochondria. J Bioenerg Biomembr, 43: 3-10.
87. Siqueira IR, Cimarosti H, Fochesatto C, Salbego C, Netto CA (2004). Age-related susceptibility to oxygen and glucose deprivation damage in rat hippocampal slices. Brain Research, 1025: 226-230.
88. Martin LJ, Adams NA, Pan Y, Price A, Wong M (2011). The Mitochondrial Permeability Transition Pore Regulates Nitric Oxide-Mediated Apoptosis of Neurons Induced by Target Deprivation. J. Neurosci., 31: 359-370.
89. Liu D, Gharavi R, Pitta M, Gleichmann M, Mattson MP (2009). Nicotinamide prevents NAD+ depletion and protects neurons against excitotoxicity and cerebral ischemia: NAD+ consumption by SIRT1 may endanger energetically compromised neurons. Neuromolecular Med, 11: 28-42.
90. Hansen AJ (1985). Effect of anoxia on ion distribution in the brain. Physiol Rev, 65: 101-48.
91. Villa RF, Gorini A, Hoyer S (2002). ATPases of synaptic plasma membranes from hippocampus after ischemia and recovery during ageing. Neurochem Res, 27: 861-70.
92. GaleffiF, Sah R, Pond BB, George A, Schwartz-Bloom RD (2004). Changes in intracellular chloride after oxygen-glucose deprivation of the adult hippocampal slice: effect of diazepam. J Neurosci, 24: 4478-88.
93. Bliss TV, Lomo T (1973). Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol, 232: 331-56.
94. Douglas RM, Goddard GV (1975). Long-term potentiation of the perforant path-granule cell synapse in the rat hippocampus. Brain Res, 86: 205-15.
95. Krug M, Lossner B, Ott T (1984). Anisomycin blocks the late phase of long-term potentiation in the dentate gyrus of freely moving rats. Brain Res Bull, 13: 39-42.
96. Nguyen PV, Abel T, Kandel ER (1994). Requirement of a critical period of transcription for induction of a late phase of LTP. Science, 265: 1104-7.
97. Barnes CA, McNaughton BL (1979). Neurophysiological comparison of dendritic cable properties in adolescent, middle-aged, and senescent rats. Exp Aging Res, 5: 195-206.
98. Barnes CA, McNaughton BL (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: 1040-8.
99. Potegal M (1969). Role of the caudate nucleus in spatial orientation of rats. J Comp Physiol Psychol, 69: 756-64.
100. Barnes CA, McNaughton BL (1980). Physiological compensation for loss of afferent synapses in rat hippocampal granule cells during senescence. J Physiol, 309: 473-85.
101. Deupree DL, Turner DA, Watters CL (1991). Spatial performance correlates with in vitro potentiation in young and aged Fischer 344 rats. Brain Research, 554: 1-9.
102. Barnes CA, Rao G, Houston FP (2000). LTP induction threshold change in old rats at the perforant path--granule cell synapse. Neurobiol Aging, 21: 613-20.
103. Landfield PW, Lynch G (1977). Impaired monosynaptic potentiation in in vitro hippocampal slices from aged, memory-deficient rats. J Gerontol, 32: 523-33.
104. Landfield PW, McGaugh JL, Lynch G (1978). Impaired synaptic potentiation processes in the hippocampus of aged, memory-deficient rats. Brain Res, 150: 85-101.
105. Barnes CA (2003). Long-term potentiation and the ageing brain. Philos Trans R Soc Lond B Biol Sci, 358: 765-72.
106. 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 U S A, 96: 5280-5.
107. Rossi MA, Mash DC, deToledo-Morrell L (2005). Spatial memory in aged rats is related to PKCgamma-dependent G-protein coupling of the M1 receptor. Neurobiol Aging, 26: 53-68.
108. Huang YY, Kandel ER (2006). Age-related enhancement of a protein synthesis-dependent late phase of LTP induced by low frequency paired-pulse stimulation in hippocampus. Learn Mem, 13: 298-306.
109. Nicoll RA (2003). Expression mechanisms underlying long-term potentiation: a postsynaptic view. Philos Trans R Soc Lond B Biol Sci, 358: 721-6.
110. Lynch G, Larson J, Kelso S, Barrionuevo G, Schottler F (1983). Intracellular injections of EGTA block induction of hippocampal long-term potentiation. Nature, 305: 719-21.
111. Malenka RC, Kauer JA, Zucker RS, Nicoll RA (1988). Postsynaptic calcium is sufficient for potentiation of hippocampal synaptic transmission. Science, 242: 81-4.
112. Nicoll RA, Kauer JA, Malenka RC (1988). The current excitement in long-term potentiation. Neuron, 1: 97-103.
113. Norris CM, Halpain S, Foster TC (1998). Reversal of age-related alterations in synaptic plasticity by blockade of L-type Ca2+ channels. J Neurosci, 18: 3171-9.
114. Tombaugh GC, Rowe WB, Chow AR, Michael TH, Rose GM (2002). Theta-frequency synaptic potentiation in CA1 in vitro distinguishes cognitively impaired from unimpaired aged Fischer 344 rats. J Neurosci, 22: 9932-40.
115. Tombaugh GC, Rowe WB, Rose GM (2005). The slow afterhyperpolarization in hippocampal CA1 neurons covaries with spatial learning ability in aged Fisher 344 rats. J Neurosci, 25: 2609-16.
116. Abdelmalik PA, Shannon P, Yiu A, Liang P, Adamchik Y, Weisspapir M, Samoilova M, McIntyre Burnham W, Carlen PL (2007). Hypoglycemic seizures during transient hypoglycemia exacerbate hippocampal dysfunction. Neurobiol Dis, 26: 646-660.
117. Izumi Y, Katsuki H, Zorumski CF (1997). Monocarboxylates (pyruvate and lactate) as alternative energy substrates for the induction of long-term potentiation in rat hippocampal slices. Neurosci Lett, 232: 17-20.
118. Sadgrove MP, Beaver CJ, Turner DA (2007). Effects of relative hypoglycemia on LTP and NADH imaging in rat hippocampal slices. Brain Res, 1165: 30-9.
119. Yamada KA, Rensing N, Izumi Y, De Erausquin GA, Gazit V, Dorsey DA, Herrera DG (2004). Repetitive hypoglycemia in young rats impairs hippocampal long-term potentiation. Pediatr Res, 55: 372-9.
120. Lisman J, Schulman H, Cline H (2002). The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci, 3: 175-90.
121. Izumi Y, Zorumski CF (1997). Involvement of nitric oxide in low glucose-mediated inhibition of hippocampal long-term potentiation. Synapse, 25: 258-62.
122. Lynch G, Rex CS, Gall CM (2007). LTP consolidation: substrates, explanatory power, and functional significance. Neuropharmacol, 52: 12-23.
123. Geinisman Y, Berry RW, Disterhoft JF, Power JM, Van der Zee EA (2001). Associative learning elicits the formation of multiple-synapse boutons. J Neurosci, 21: 5568-73.
124. Nicholson DA, Yoshida R, Berry RW, Gallagher M, Geinisman Y (2004). Reduction in size of perforated postsynaptic densities in hippocampal axospinous synapses and age-related spatial learning impairments. J Neurosci, 24: 7648-53.
125. Barnes CA, Rao G, Foster TC, McNaughton BL (1992). Region-specific age effects on AMPA sensitivity: electrophysiological evidence for loss of synaptic contacts in hippocampal field CA1. Hippocampus, 2: 457-68.
126. Ekstrom AD, Meltzer J, McNaughton BL, Barnes CA (2001). NMDA receptor antagonism blocks experience-dependent expansion of hippocampal "place fields". Neuron, 31: 631-8.
127. Boric K, Munoz P, Gallagher M, Kirkwood A (2008). Potential adaptive function for altered long-term potentiation mechanisms in aging hippocampus. J Neurosci, 28: 8034-9.
128. Collingridge GL, Kehl SJ, McLennan H (1983). Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J Physiol, 334: 33-46.
129. Collingridge GL, Kehl SJ, McLennan H (1983). The antagonism of amino acid-induced excitations of rat hippocampal CA1 neurones in vitro. J Physiol, 334: 19-31.
130. Washbourne P, Bennett JE, McAllister AK (2002). Rapid recruitment of NMDA receptor transport packets to nascent synapses. Nat Neurosci, 5: 751-9.
131. Washbourne P, Liu XB, Jones EG, McAllister AK (2004). Cycling of NMDA receptors during trafficking in neurons before synapse formation. J Neurosci, 24: 8253-64.
132. Grosshans DR, Browning MD (2001). Protein kinase C activation induces tyrosine phosphorylation of the NR2A and NR2B subunits of the NMDA receptor. J Neurochem, 76: 737-44.
133. Deupree DL, Bradley J, Turner DA (1993). Age-related alterations in potentiation in the CA1 region in F344 rats. Neurobiol Aging, 14: 249-58.
134. Barnes CA, Rao G, McNaughton BL (1987). Increased electrotonic coupling in aged rat hippocampus: a possible mechanism for cellular excitability changes. J Comp Neurol, 259: 549-58.
135. 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: 154-62.
136. Malenka RC, Nicoll RA (1999). Long-term potentiation--a decade of progress? Science, 285: 1870-4.
137. Gustafsson B, Wigstrom H (1988). Physiological mechanisms underlying long-term potentiation. Trends Neurosci, 11: 156-62.
138. Bliss TV, Collingridge GL (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature, 361: 31-9.
139. Gustafsson B, Wigstrom H, Abraham WC, Huang YY (1987). Long-term potentiation in the hippocampus using depolarizing current pulses as the conditioning stimulus to single volley synaptic potentials. J Neurosci, 7: 774-80.
140. Lau CG, Zukin RS, Lau CG, Zukin RS (2007). NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders. Nature Reviews Neuroscience, 8: 413-26.
141. Lister JP, Barnes CA (2009). Neurobiological changes in the hippocampus during normative aging. Arch Neurol, 66: 829-33.
142. Norris CM, Korol DL, Foster TC (1996). Increased susceptibility to induction of long-term depression and long-term potentiation reversal during aging. J Neurosci, 16: 5382-92.
143. Fukunaga K, Muller D, Miyamoto E (1996). CaM kinase II in long-term potentiation. Neurochem Int, 28: 343-58.
144. Song I, Huganir RL (2002). Regulation of AMPA receptors during synaptic plasticity. Trends Neurosci, 25: 578-88.
145. Shetty PK, Huang FL, Huang KP (2008). Ischemia-elicited oxidative modulation of Ca2+/calmodulin-dependent protein kinase II. J Biol Chem, 283: 5389-401.
146. Robison AJ, Winder DG, Colbran RJ, Bartlett RK (2007). Oxidation of calmodulin alters activation and regulation of CaMKII. Biochem Biophys Res Commun, 356: 97-101.
147. Huang KP, Huang FL, Shetty PK, Yergey AL (2007). Modification of protein by disulfide S-monoxide and disulfide S-dioxide: distinctive effects on PKC. Biochemistry, 46: 1961-71.
148. Foster TC, Foster TC (2006). Biological markers of age-related memory deficits: treatment of senescent physiology. CNS Drugs, 20: 153-66.
149. Poon HF, Shepherd HM, Reed TT, Calabrese V, Stella AM, Pennisi G, Cai J, Pierce WM, Klein JB, Butterfield DA (2006). Proteomics analysis provides insight into caloric restriction mediated oxidation and expression of brain proteins associated with age-related impaired cellular processes: Mitochondrial dysfunction, glutamate dysregulation and impaired protein synthesis. Neurobiol Aging, 27: 1020-34.
150. Parihar MS, Brewer GJ (2007). Simultaneous age-related depolarization of mitochondrial membrane potential and increased mitochondrial reactive oxygen species production correlate with age-related glutamate excitotoxicity in rat hippocampal neurons. J Neurosci Res, 85: 1018-32.
151. Parihar MS, Kunz EA, Brewer GJ (2008). Age-related decreases in NAD(P)H and glutathione cause redox declines before ATP loss during glutamate treatment of hippocampal neurons. J Neuroscie Res, 86: 2339-52.
152. Rebrin I, Forster MJ, Sohal RS (2007). Effects of age and caloric intake on glutathione redox state in different brain regions of C57BL/6 and DBA/2 mice. Brain Res, 1127: 10-8.
153. Liu RM, Liu R-M (2002). Down-regulation of gamma-glutamylcysteine synthetase regulatory subunit gene expression in rat brain tissue during aging. J Neurosci Res, 68: 344-51.
154. Lee MS, Kwon YT, Li M, Peng J, Friedlander RM, Tsai LH (2000). Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature, 405: 360-4.
155. Qu D, Rashidian J, Mount MP, Aleyasin H, Parsanejad M, Lira A, Haque E, Zhang Y, Callaghan S, Daigle M, Rousseaux MW, Slack RS, Albert PR, Vincent I, Woulfe JM, Park DS (2007). Role of Cdk5-mediated phosphorylation of Prx2 in MPTP toxicity and Parkinson's disease. Neuron, 55: 37-52.
156. Sun KH, de Pablo Y, Vincent F, Shah K (2008). Deregulated Cdk5 promotes oxidative stress and mitochondrial dysfunction. J Neurochem, 107: 265-78.
157. Kim MJ, Oh SJ, Park SH, Kang HJ, Won MH, Kang TC, Park JB, Kim JI, Kim J, Lee JY (2007). Neuronal loss in primary long-term cortical culture involves neurodegeneration-like cell death via calpain and p35 processing, but not developmental apoptosis or aging. Exp Mol Med, 39: 14-26.
158. Cataldo AM, Broadwell RD (1986). Cytochemical identification of cerebral glycogen and glucose-6-phosphatase activity under normal and experimental conditions. II. Choroid plexus and ependymal epithelia, endothelia and pericytes. J Neurocytol, 15: 511-24.
159. Choi IY, Seaquist ER, Gruetter R (2003). Effect of hypoglycemia on brain glycogen metabolism in vivo. J Neurosci Res, 72: 25-32.
160. Brown AM, Sickmann HM, Fosgerau K, Lund TM, Schousboe A, Waagepetersen HS, Ransom BR (2005). Astrocyte glycogen metabolism is required for neural activity during aglycemia or intense stimulation in mouse white matter. J Neurosci Res, 79: 74-80.
161. Suh SW, Aoyama K, Matsumori Y, Liu J, Swanson RA (2005). Pyruvate Administered After Severe Hypoglycemia Reduces Neuronal Death and Cognitive Impairment. Diabetes, 54: 1452-1458.
162. Shen H, Hu X, Liu C, Wang S, Zhang W, Gao H, Stetler RA, Gao Y, Chen J (2010). Ethyl pyruvate protects against hypoxic-ischemic brain injury via anti-cell death and anti-inflammatory mechanisms. Neurobiol Dis, 37: 711-722.
163. Balestrino M, Rebaudo R, Lunardi G (1999). Exogenous creatine delays anoxic depolarization and protects from hypoxic damage: dose-effect relationship. Brain Res, 816: 124-30.
164. Brustovetsky N, Brustovetsky T, Dubinsky JM (2001). On the mechanisms of neuroprotection by creatine and phosphocreatine. J Neurochem, 76: 425-34.
165. Tarnopolsky MA, Beal MF (2001). Potential for creatine and other therapies targeting cellular energy dysfunction in neurological disorders. Ann Neurol, 49: 561-74.
166. Calabrese V, Colombrita C, Sultana R, Scapagnini G, Calvani M, Butterfield DA, Stella AM (2006). Redox modulation of heat shock protein expression by acetylcarnitine in aging brain: relationship to antioxidant status and mitochondrial function. Antioxid Redox Signal, 8: 404-16.
167. Liu D, Pitta M, Mattson MP (2008). Preventing NAD(+) depletion protects neurons against excitotoxicity: bioenergetic effects of mild mitochondrial uncoupling and caloric restriction. Ann N Y Acad Sci, 1147: 275-82.
168. Canto C, Gerhart-Hines Z, Feige JN, Lagouge M, Noriega L, Milne JC, Elliott PJ, Puigserver P, Auwerx J (2009). AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature, 458: 1056-60.
169. Duan W, Ross CA (2010). Potential therapeutic targets for neurodegenerative diseases: lessons learned from calorie restriction. Curr Drug Targets, 11: 1281-92.
170. Fontana L, Partridge L, Longo VD (2010). Extending healthy life span--from yeast to humans. Science, 328: 321-6.
171. Morley JE, Chahla E, Alkaade S (2010). Antiaging, longevity and calorie restriction. Curr Opin Clin Nutr Metab Care, 13: 40-5.
172. Smith DL, Jr., Nagy TR, Allison DB (2010). Calorie restriction: what recent results suggest for the future of ageing research. Eur J Clin Invest, 40: 440-50.
173. Someya S, Yu W, Hallows WC, Xu J, Vann JM, Leeuwenburgh C, Tanokura M, Denu JM, Prolla TA (2010). Sirt3 mediates reduction of oxidative damage and prevention of age-related hearing loss under caloric restriction. Cell, 143: 802-12.
174. Lanza IR, Nair KS (2010). Mitochondrial function as a determinant of life span. Pflugers Arch, 459: 277-89.
175. Mookerjee SA, Divakaruni AS, Jastroch M, Brand MD (2010). Mitochondrial uncoupling and lifespan. Mech Ageing Dev, 131: 463-72.
176. Lu T, Pan Y, Kao SY, Li C, Kohane I, Chan J, Yankner BA (2004). Gene regulation and DNA damage in the ageing human brain. Nature, 429: 883-91.
177. Mattson MP, Wan R (2005). Beneficial effects of intermittent fasting and caloric restriction on the cardiovascular and cerebrovascular systems. J Nutr Biochem, 16: 129-37.
178. Khanna A, Muthusamy S, Liang R, Sarojini H, Wang E (2011). Gain of survival signaling by down-regulation of three key miRNAs in brain of calorie-restricted mice. Aging (Albany NY), 3: 223-36.
179. Li Y, Tollefsbol TO (2011). p16 Suppression by Glucose Restriction Contributes to Human Cellular Lifespan Extension through SIRT1-Mediated Epigenetic and Genetic Mechanisms. PLoS One, 6: e17421.
180. Bruce-Keller AJ, Umberger G, McFall R, Mattson MP (1999). Food restriction reduces brain damage and improves behavioral outcome following excitotoxic and metabolic insults. Ann Neurol, 45: 8-15.
181. Kendall DM, Harmel AP (2002). The metabolic syndrome, type 2 diabetes, and cardiovascular disease: understanding the role of insulin resistance. Am J Manag Care, 8: S635-53; quiz S654-7.
182. Spaulding CC, Walford RL, Effros RB (1997). Calorie restriction inhibits the age-related dysregulation of the cytokines TNF-alpha and IL-6 in C3B10RF1 mice. Mech Ageing Dev, 93: 87-94.
183. Heilbronn LK, Ravussin E (2003). Calorie restriction and aging: review of the literature and implications for studies in humans. Am J Clin Nutr, 78: 361-9.
184. Pamplona R, Portero-Otin M, Requena J, Gredilla R, Barja G (2002). Oxidative, glycoxidative and lipoxidative damage to rat heart mitochondrial proteins is lower after 4 months of caloric restriction than in age-matched controls. Mech Ageing Dev, 123: 1437-46.
185. Sohal RS, Agarwal S, Candas M, Forster MJ, Lal H (1994). Effect of age and caloric restriction on DNA oxidative damage in different tissues of C57BL/6 mice. Mech Ageing Dev, 76: 215-24.
186. Yu ZF, Mattson MP (1999). Dietary restriction and 2-deoxyglucose administration reduce focal ischemic brain damage and improve behavioral outcome: evidence for a preconditioning mechanism. J Neurosci Res, 57: 830-9.
187. Young JB, Mullen D, Landsberg L (1978). Caloric restriction lowers blood pressure in the spontaneously hypertensive rat. Metabolism, 27: 1711-4.
188. Wan R, Camandola S, Mattson MP (2003). Intermittent food deprivation improves cardiovascular and neuroendocrine responses to stress in rats. J Nutr, 133: 1921-9.
189. Deary IJ, Corley J, Gow AJ, Harris SE, Houlihan LM, Marioni RE, Penke L, Rafnsson SB, Starr JM (2009). Age-associated cognitive decline. Br Med Bull, 92: 135-52.
190. Van Dyk K, Sano M (2007). The impact of nutrition on cognition in the elderly. Neurochem Res, 32: 893-904.
191. Parrott MD, Greenwood CE (2007). Dietary influences on cognitive function with aging: from high-fat diets to healthful eating. Ann N Y Acad Sci, 1114: 389-97.
192. Fratiglioni L, Paillard-Borg S, Winblad B (2004). An active and socially integrated lifestyle in late life might protect against dementia. Lancet Neurol, 3: 343-53.
193. Lee J, Duan W, Mattson MP (2002). Evidence that brain-derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice. J Neurochem, 82: 1367-75.
194. Tan SE, Wenthold RJ, Soderling TR (1994). Phosphorylation of AMPA-type glutamate receptors by calcium/calmodulin-dependent protein kinase II and protein kinase C in cultured hippocampal neurons. J Neurosci, 14: 1123-9.
195. Nicholls DG (2002). Mitochondrial function and dysfunction in the cell: its relevance to aging and aging-related disease. Int J Biochem Cell Biol, 34: 1372-1381.
196. Tielen AM, Mollevanger WJ, Lopes da Silva FH, Hollander CF (1983). Neuronal plasticity in hippocampal slices of extremely old rats. In: Gipsen WH, Traber J. (Eds). Aging of the brain. Elsevier, Amsterdam, pp. 73-84.
197. Shankar S, Teyler TJ, Robbins N (1998). Aging differentially alters forms of long-term potentiation in rat hippocampal area CA1. J Neurophysiol, 79: 334-41.
198. Grover LM, Teyler TJ (1990). Two components of long-term potentiation induced by different patterns of afferent activation. Nature, 347: 477-9.