Neurobiology of Aging
Volume 24, Issue 1 , Pages 37-48 , January 2003

Age-related deficits as working memory load increases: relationships with growth factors

Received 24 September 2001 ,Revised 1 February 2002 ,Accepted 1 February 2002.

References 

  1. Aggleton JP, Blindt HS, Candy JM. Working memory in aged rats. Behav. Neurosci. 1989;103(5):975–983
  2. Almli C, Levy T, Hee Han B, Shah A, Gidday J, Holtzman D. BDNF protects against spatial memory deficits following neonatal hypoxia–ischemia. Exp. Neurol. 2000;166:99–114
  3. Arendash GW, Sanberg PR, Sengstock GJ. Nicotine enhances the learning and memory of aged rats. Pharm. Biochem. Behav. 1995;52(3):517–523
  4. Armstrong DM, Sheffield R, Buzsaki G, Chen KS, Hersh LB, Nearing B, et al.  Morphologic alterations of choline acetyltransferase-positive neurons in the basal forebrain of aged behaviorally characterized Fischer 344 rats. Neurobiol. Aging. 1993;14:457–470
  5. Backman C, Rose GM, Hoffer BJ, Henry MA, Bartus RT, Friden P, et al.  Systemic administration of nerve growth factor conjugate reverses age-related cognitive dysfuction and prevents cholinergic neuron atrophy. J. Neurosci. 1996;16(17):5437–5442
  6. Barnes CA, Nadel L, Honig WK. Spatial memory deficit in senescent rats. Can. J. Psychol. 1980;34(1):29–39
  7. Bartus RT, Dean RL, Beer B, Lippa AS. The cholinergic hypothesis of geriatric memory dysfunction. Science. 1982;217(4558):408–414
  8. Beatty WW, Bierley RA, Boyd JG. Preservation of accurate spatial memory in aged rats. Neurobiol. Aging. 1985;6:219–225
  9. Biegon A, Greenberger V, Segal M. Quantitative histochemistry of brain acetylcholinesterase and learning rate in the aged rat. Neurobiol. Aging. 1986;7:215–217
  10. Bimonte H, Denenberg V. Sex differences in vicarious trial-and-error behavior during radial-arm maze learning. Physiol. Behav. 2000;68:495–499
  11. Bimonte H, Hyde L, Hoplight B, Denenberg V. In two species, females exhibit superior working memory and inferior reference memory on the water radial-arm maze. Physiol. Behav. 2000;70:311–317
  12. Bimonte HA, Denenberg VH. Estradiol facilitates performance as working memory load increases. Psychoneuroendocrin. 1999;24(2):161–173
  13. Bond NW, Everitt AV, Walton J. Effects of dietary restriction on radial-arm maze performance and flavor memory in aged rats. Neurobiol. Aging. 1989;10:27–30
  14. Chrobak JJ, Hanin I, Lorens SA, Napier TC. Within subject decline in delayed-non-match-to-sample radial-arm maze performance in aging Sprague–Dawley rats. Behav. Neurosci. 1995;109:241–245
  15. Craik F. Memory functions in normal aging. In: Yanagihara T, Petersen R, editors. Memory disorders: research and clinical practice. New York: Marcel Dekker, 1991. p. 347–67.
  16. Croll SD, Chesnutt CR, Greene NA, Lindsay RM, Weigand SJ. Peptide immunoreactivity in aged rat cortex and hippocampus as a function of memory and BDNF infusion. Pharmacol. Biochem. Behav. 1999;64(3):625–635
  17. Croll SD, Ip NY, Lindsay RM, Wiegand SJ. Expression of BDNF and trkB as a function of age and cognitive performance. Brain Res. 1998;812:200–208
  18. Denenberg VH. A primer for behavioral research. Mental Retard. Dev. Disab. Res. Rev. 1996;2:209–215
  19. DeRonchi D, Fratiglioni L, Rucci P, Paternico A, Graziani S, Dalmonte E. The effect of education on dementia occurrence in an Italian population with middle to high socio-economic status. Neurology. 1998;50:1231–1238
  20. Diana G, Domenici MR, Scotti de Caroli A, Loizzo A, Sagratella S. Reduced hippocampal CA1 Ca2+-induced long-term potentiation is associated with age-dependent impairment of spatial learning. Brain Res. 1995;686:107–110
  21. Dixon CE, Flinn P, Bao J, Venya R, Hayes RL. Nerve growth factor attenuates cholinergic deficits following traumatic brain injury in rats. Exp. Neurobiol. 1997;146:479–490
  22. Drachman D, Leavitt J. Human memory and the cholinergic system: a relationship to aging?. Arch. Neurol. 1974;30:113–121
  23. Dunnet SB, Evenden JL, Iversen SD. Delay-dependent short-term memory deficits in aged rats. Psychopharmacology. 1988;96:174–180
  24. Eckerman DA, Gordon WA, Edwards JD, MacPhail RC, Gage MI. Effects of scopolamine, pentobarbital, and amphetamine on radial-arm maze performance in the rat. Pharmacol. Biochem. Behav. 1980;12(4):595–602
  25. Fischer W, Bjorklund A, Chen K, Gage FH. NGF improves spatial memory in aged rodents as a function of age. J. Neurosci. 1991;11(7):1889–1906
  26. Fischer W, Sirevaag A, Wiegand S, Lindsay R, Bjorklund A. Reversal of spatial memory impairments in aged rats by nerve growth factor and neurotrophins 3 and 4/5 but not by brain-derived neurotrophic factor. Proc. Natl. Acad. Sci. U.S.A. 1994;91:8607–8611
  27. Fischer W, Wictorin K, Bjorklund A, Williams LR, Varon S, Gage FH. Amelioration of cholinergic neuron atrophy and spatial memory impairment in aged rats by nerve growth factor. Nature. 1987;329(3):65–68
  28. Frick KM, Baxter MG, Markowska AL, Olton DS, Price DL. Age-related spatial reference and working memory deficits assessed in the water maze. Neurobiol. Aging. 1995;16(2):149–160
  29. Frick KM, Price DL, Koliatsos VE, Markowska AL. The effects of nerve growth factor on spatial recent memory in aged rats persist after discontinuation of treatment. J. Neurosci. 1997;17(7):2543–2550
  30. Funahashi S, Kubota K. Working memory and prefrontal cortex. Neurosci. Res. 1994;21:1–11
  31. Gage FH, Dunnett SB, Bjorklund A. Spatial learning and motor deficits in aged rats. Neurobiol. Aging. 1984;5:43–48
  32. Gallagher M, Burwell RD. Relationship of age-related decline across several behavioral domains. Neurobiol. Aging. 1989;10:691–708
  33. Gallagher M, Burwell R, Burchinal M. Severity of spatial learning impairment in aging: development of a learning index for performance in the Morris water maze. Behav. Neurosci. 1993;107(4):618–626
  34. Gallagher M, Burwell RD, Kodsi MH, McKinney M, Southerland S, Vella-Rountree L, et al.  Markers for biogenic amines in the aged rat brain: relationship to decline in spatial learning ability. Neurobiol. Aging. 1990;11:507–514
  35. Gibbs RB, Aggarwal P. Estrogen and basal forebrain cholinergic neurons: implications for brain aging and Alzheimer’s disease-related cognitive decline. Horm. Behav. 1998;34:98–111
  36. Granholm AC. Oestrogen and nerve growth factor- neuroprotection and repair in Alzheimer’s disease. Exp. Opin. Invest Drugs. 2000;9(4):1–10
  37. Gustilo MC, Markowska AL, Breckler SJ, Fleischsman CA, Price DL, Koliatsos VE. Evidence that nerve growth factor influences recent memory through structural changes in septohippocampal cholinergic neurons. J. Compar. Neurol. 1999;405:491–507
  38. Hasenohrl RU, Soderstrom S, Mohammed AH, Eberdal T, Huston JP. Reciprocal changes in expression of mRNA for nerve growth factor and its receptors TrkA and LNGFR in brain of aged rats in relation to maze learning deficits. Exp. Brain Res. 1997;114:205–213
  39. Hyde L, Sherman G, Denenberg V. Non-spatial water radial-arm maze learning in mice. Brain Res. 2000;863:151–159
  40. Hyde LA, Hoplight BJ, Denenberg VH. Water version of the radial-arm maze: learning in three inbred strains of mice. Brain Res. 1998;785(2):236–244
  41. Ickes BR, Pham TM, Sanders LA, Albeck DS, Mohammed AH, Granholm A-Ch. Long-term environmental enrichment leads to regional increases in neurotrophin levels in rat brain. Exp. Neurol. 2000;164:45–52
  42. Jarrard L, Okaichi H, Steward O, Goldschmidt R. On the role of hippocampal connections in the performance of place and cue tasks: comparisons with damage to hippocampus. Behav. Neurosci. 1984;98(6):946–954
  43. Kadar T, Arbel I, Silbermann M, Levy A. Morphological hippocampal changes during normal aging and their relation to cognitive deterioration. J. Neural. Transm. 1994;44:133–143
  44. Kaisho Y, Ohta H, Miyamato M, Igarashi K. Nerve growth factor promoter driven neurotrophin-3 overexpression in the mouse and the neuroprotective effects of transgene on age-related behavioral deficits. Neurosci. Lett. 1999;277:181–184
  45. Koh S, Chang P, Collier TJ, Loy R. Loss of NGF receptor immunoreactivity in basal forebrain neurons of aged rats: correlation with spatial memory impairment. Brain Res. 1989;498:397–404
  46. Levi-Montalcini R. The nerve growth factor 35 years later. Science. 1987;237:1154–1162
  47. Levin ED, Torry D. Acute and chronic nicotine effects on working memory in aged rats. Psychopharmacology. 1996;123:88–97
  48. Levin ED, Wilkerson A, Jones JP, Christopher NC, Briggs SJ. Prenatal nicotine effects on memory in rats: pharmacological and behavioral challenges. Dev. Brain Res. 1996;97(2):207–215
  49. Lindner MD. Reliability, distribution, and validity of age-related cognitive deficits in the Morris water maze. Neurobiol. Learn Mem. 1997;68:203–220
  50. Lindner MD, Balch AH, Vandermaelen CP. Short forms of the “reference-” and “working-memory” Morris water maze for assessing age-related deficits. Behav. Neural. Biol. 1992;58:94–102
  51. Lindner MD, Kearns CE, Winn SR, Frydel B, Emerich DF. Effects in intraventricular encapsulated hNGF-secreting fibroblasts in aged rats. Cell Transplant. 1996;5(2):205–223
  52. Luine V, Hearns M. Spatial memory deficits in aged rats: contributions of the cholinergic system assessed by ChAT. Brain Res. 1990;523:321–324
  53. Luine V, Renner K, Heady S, Jones K. Age- and sex-dependent decreases in ChAT in basal forebrain nuclei. Neurobiol. Aging. 1986;7:193–198
  54. Markowska AL. Sex dimorphisms in the rate of age-related decline in spatial memory: relevance to alterations in the estrous cycle. J. Neurosci. 1999;19(18):8122–8133
  55. Markowska AL, Koliatsos VE, Breckler SJ, Price DL, Olton DS. Human nerve growth factor improves spatial memory in aged but not in young rats. J. Neurosci. 1994;14(8):4815–4824
  56. Markowska AL, Stone WS, Ingram DK, Reynolds J, Gold PE, Conti LH, et al.  Individual differences in aging: behavioral and neurobiological correlates. Neurobiol. Aging. 1989;10:31–43
  57. Meites J, Lu JK. Reproductive ageing and neuroendocrine function. In: Charlton HM, editor. Oxford reviews of reproductive biology, 1994. p. 215–39.
  58. Mesches M, Juthberg S, Albeck D, Browning M, Bickford P, Rose G, Granholm A-Ch. Is cognitive status during aging dependent upon a reciprocal relationship between NGF in basal forebrain and hippocampus? (Submitted).
  59. Mizuno M, Yamada K, Olariu A, Nawa H, Nabeshima T. Involvement of brain-derived neurotrophic factor in spatial memory formation and maintenance in a radial-arm maze test in rats. J. Neurosci. 2000;20(18):7116–7121
  60. Mufson EJ, Conner JM, Kordower J. Nerve growth factor in Alzheimer’s disease: defective retrograde transport to nucleus basalis. NeuroReport. 1995;6:1063–1066
  61. Muir JL. Acetylcholine, aging, and Alzheimer’s disease. Pharmacol. Biochem. Behav. 1997;56(4):687–696
  62. Nilsson OG, Gage FH. Anticholinergic sensitivity in the aging rat septohippocampal system as assessed in a spatial memory task. Neurobiol. Aging. 1993;14:487–497
  63. Nishizuka M, Katoh-Semba R, Eto K, Arai Y, IIzuka R, Kato K. Age- and sex-related differences in the nerve growth factor distribution in the rat brain. Brain Res. Bull. 1991;27:685–688
  64. Noda Y, Yamada K, Nabeshima T. Role of nitric oxide in the effect of aging on spatial memory in rats. Behav. Brain Res. 1997;83:153–158
  65. Ohkura T, Isse K, Akazawa K, Hamamoto M, Yaoi Y, Hagino N. Long-term estrogen replacement therapy in female patients with dementia of the Alzheimer type: seven case reports. Dementia. 1995;6(2):99–107
  66. Olton D. Characteristics of spatial memory. In: Hulse S, Fowler H, Honig W, editors. Cognitive processes in animal behavior. Hilldale: Erlbaum, 1978. p. 341–73.
  67. Olton D, Becker J, Handelmann G. Hippocampus, space, and memory. Behav. Brain Sci. 1979;2:313–365
  68. Olton D, Samuelson R. Remembrance of places passed: spatial memory in rats. J. Exp. Psychol.: Anim. Behav. Process. 1976;2:97–116
  69. Ott A, Van Rossum C, Van Harskamp F, Van de Mheen H, Hofman A, Breteler M. Education and the incidence of dementia in a large population based study: the Rotterdam Study. Neurology. 1999;52:663–666
  70. Pham TM, Ickes B, Albeck D, Soderstrom S, Granholm A-Ch, Mohammed AH. Changes in brain nerve growth factor levels and nerve growth factor receptors in rat exposed to environmental enrichment for 1 year. Neuroscience. 1999;94(1):279–286
  71. Pham TM, Soderstrom S, Winbald B, Mohammed AH. Effects of environmental enrichment on cognitive function and hippocampal NGF in the nonhandled rats. Behav. Brain Res. 1999;103:63–70
  72. Pitsikas N, Algeri S. Deterioration of spatial and nonspatial reference and working memory in aged rats: protective effect of life-long calorie restriction. Neurobiol. Aging. 1992;13:369–373
  73. Quirion R, Wilson A, Rowe W, Aubert I, Richard J, Doods H, et al.  Facilitation of acetylcholine release and cognitive performance by an M(2)-muscarinic receptor antagonist in aged memory-impaired rats. J. Neurosci. 1995;15:1455–1462
  74. Rapp PR, Gallagher M. Preserved neuron number in the hippocampus of aged rats with spatial learning deficits. Neurobiology. 1996;93:9926–9930
  75. Rapp PR, Rosenberg RA, Gallagher M. An evaluation of spatial information processing in aged rats. Behav. Neurosci. 1987;101:3–12
  76. Reisberg B, editor. Alzheimer’s disease. New York: Free Press, 1983.
  77. Rupniak NM, Samson NA, Steventon MJ, Iversen SD. Induction of cognitive impairment by scopolamine and noncholinergic agents in rhesus monkeys. Life Sci. 1991;48(9):893–899
  78. Scali C, Casamenti F, Pazzagli M, Bartolini L, Pepeu G. Nerve growth factor increases extracellular acetylcholine levels in the parietal cortex and hippocampus of aged rats and restores object recognition. Neurosci. Lett. 1994;170:117–120
  79. Siegel GJ, Chauhan N. Neurotrophic factors in Alzheimer’s and Parkinson’s disease brains. Brain Res. Rev. 2000;33:199–227
  80. Stewart J, Mitchell J, Kalant N. The effects of life-long food restriction of spatial memory in young and aged Fischer 344 rats measured in the eight-arm radial and Morris water mazes. Neurobiol. Aging. 1989;10:669–675
  81. Sugaya K, Greene R, Personett D, Robbins M, Kent C, Bryan D, et al.  Septo-hippocampal cholinergic and neurotrophin markers in age-induced cognitive decline. Neurobiol. Aging. 1998;19(4):351–361
  82. Torasdotter M, Metsis M, Henrikson BG, Winbald B, Mohammed AH. Environmental enrichment results in higher levels of nerve growth factor mRNA in the rat visual cortex and hippocampus. Behav. Brain Res. 1998;93:83–90
  83. Torasdotter M, Metsis M, Henriksson BG, Winbald B, Mohammed AH. Expression of neurotropin-3 mRNA in the rat visual cortex and hippocampus is influenced by environmental conditions. Neurosci. Lett. 1996;218:107–110
  84. Ueyama T, Yoshinori K, Nemoto K, Sekimoto M, Tone S, Senba E. Immobilization stress reduced the expression of neurotrophins and their receptors in the rat brain. Neurosci. Res. 1997;28:103–110
  85. Wallace JE, Krauter EE, Campbell BA. Animals models of declining memory in the aged: short-term and spatial memory in the aged rat. J. Gerontol. 1980;35:355–363
  86. Ward MT, Stoelzel CR, Markus EJ. Hippocampal dysfunction during aging II:K deficits on the radial-arm maze. Neurobiol. Aging. 1999;20:373–380
  87. Warren SG, Juraska J. Sex differences and estropausal phase effects on water maze performance in aged rats. Neurobiol. Learn Mem. 2000;74:229–240
  88. Wellman C, Pelleymounter MA. Differential effects of nucleus basalis lesions in young adult and aging rat. Neurobiol. Aging. 1999;20:381–393
  89. Willig F, Palacios A, Monmar P, M’Harzi M, Laurent J, Delacour J. Short-term memory, exploration and locomotor activity in aged rats. Neurobiol. Aging. 1987;8:393–402
  90. Winocur G. The effects of retroactive and proactive interference on learning and memory in old and young rats. Dev. Psychobiol. 1984;17(5):537–545
  91. Winocur G. Memory decline in aged rats: a neuropsychological interpretation. J. Gerentol. 1986;41(6):758–763
  92. Woolf N. Cholinergic systems in mammalian brain and spinal cord. Prog. Neurobiol. 1991;37:475–524
  93. Zornetzer SF, Thompson R, Rogers J. Rapid forgetting in aged rats. Behav. Neurol. Biol. 1982;36:49–60

PII: S0197-4580(02)00015-5

Neurobiology of Aging
Volume 24, Issue 1 , Pages 37-48 , January 2003

Article Tools

* Image Usage & Resolution