Learning to remember: Cognitive training-induced attenuation of age-related memory decline depends on sex and cognitive demand, and can transfer to untrained cognitive domains

Neurobiology of Aging

Volumn 35, Issue 12, 2014, Pages 2791-2802

  Talboom, Joshua S ^a,b   West, Stephen G ^a,b   Engler Chiurazzi, Elizabeth B ^a,b   Enders, Craig K ^a   Crain, Ian ^a   Bimonte Nelson, Heather A ^a,b  

^a ARIZONA STATE UNIVERSITY   (United States)

^b ARIZONA ALZHEIMER S CONSORTIUM   (United States)

Author keywords

Age related memory decline; Aging; Cognitive training; Enrichment; Learning; Memory; Neurobics; Spatial

Indexed keywords

NEUROTROPHIN; NERVE GROWTH FACTOR;

ADULT; AGE DISTRIBUTION; AGED; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COGNITION; COGNITIVE TRAINING; CONTROLLED STUDY; FEMALE; LEARNING; MALE; MEMORY DISORDER; MENTAL DETERIORATION; MENTAL PERFORMANCE; MENTAL TASK; NONHUMAN; RAT; SEX; SEX DIFFERENCE; SPATIAL MEMORY; T-MAZE TEST; TRAINING; ANIMAL; BRAIN; FISCHER 344 RAT; LONGITUDINAL STUDY; MAZE TEST; MEMORY DISORDERS; METABOLISM; PHYSIOLOGY; PSYCHOLOGY; SEXUAL DEVELOPMENT;

AGING; ANIMALS; BRAIN; COGNITION; FEMALE; LONGITUDINAL STUDIES; MALE; MAZE LEARNING; MEMORY DISORDERS; NERVE GROWTH FACTORS; RATS, INBRED F344; SEX CHARACTERISTICS; SPATIAL MEMORY;

EID: 84911383693     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.06.008     Document Type: Article

References (81)

1. Acosta J.I., Mayer L., Talboom J.S., Tsang C.W., Smith C.J., Enders C.K., Bimonte-Nelson H.A. Transitional versus surgical menopause in a rodent model: etiology of ovarian hormone loss impacts memory and the acetylcholine system. Endocrinology 2009, 150:4248-4259.
2. Acosta J.I., Mayer L., Talboom J.S., Zay C., Scheldrup M., Castillo J., Demers L.M., Enders C.K., Bimonte-Nelson H.A. Premarin improves memory, prevents scopolamine-induced amnesia and increases number of basal forebrain choline acetyltransferase positive cells in middle-aged surgically menopausal rats. Horm. Behav. 2009, 55:454-464.
3. Ando S., Ohashi Y. Longitudinal study on age-related changes of working and reference memory in the rat. Neurosci. Lett. 1991, 128:17-20.
4. Anguera J.A., Boccanfuso J., Rintoul J.L., Al-Hashimi O., Faraji F., Janowich J., Kong E., Larraburo Y., Rolle C., Johnston E., Gazzaley A. Video game training enhances cognitive control in older adults. Nature 2013, 501:97-101. http://www.nature.com/nature/journal/v501/n7465/abs/nature12486.html#supplementary-information, 10.1038/nature12486.
5. Association, A.V.M. 2007. AVMA Guidelines on Euthanasia (Formerly Report of the AVMA Panel on Euthanasia): Jun 2007 update. Available from . http://www.avma.org/issues/animal_welfare/euthanasia%20pdf.
6. Backman C., Rose G.M., Hoffer B.J., Henry M.A., Bartus R.T., Friden P., Granholm A.C. Systemic administration of a nerve growth factor conjugate reverses age-related cognitive dysfunction and prevents cholinergic neuron atrophy. J.Neurosci. 1996, 16:5437-5442.
7. Ballard C., Gauthier S., Corbett A., Brayne C., Aarsland D., Jones E. Alzheimer's disease. Lancet 2011, 377:1019-1031.
8. Barnes C.A., Nadel L., Honig W.K. Spatial memory deficit in senescent rats. Can. J. Psychol. 1980, 34:29-39.
9. Bierley R.A., Rixen G.J., Troster A.I., Beatty W.W. Preserved spatial memory in old rats survives 10 months without training. Behav. Neural Biol. 1986, 45:223-229.
10. Bimonte-Nelson H.A., Granholm A.C., Nelson M.E., Moore A.B. Patterns of neurotrophin protein levels in male and female Fischer 344 rats from adulthood to senescence: how young is "young" and how old is "old"?. Exp. Aging Res. 2008, 34:13-26.
11. Bimonte-Nelson H.A., Hunter C.L., Nelson M.E., Granholm A.-C.E. Frontal cortex BDNF levels correlate with working memory in an animal model of Down syndrome. Behav. Brain Res. 2003, 139:47-57.
12. Bimonte-Nelson H.A., Singleton R.S., Hunter C.L., Price K.L., Moore A.B., Granholm A.C. Ovarian hormones and cognition in the aged female rat: I. Long-term, but not short-term, ovariectomy enhances spatial performance. Behav. Neurosci. 2003, 117:1395-1406.
13. Bimonte-Nelson H.A., Singleton R.S., Nelson M.E., Eckman C.B., Barber J., Scott T.Y., Granholm A.C. Testosterone, but not nonaromatizable dihydrotestosterone, improves working memory and alters nerve growth factor levels in aged male rats. Exp. Neurol. 2003, 181:301-312.
14. Bimonte-Nelson H.A., Singleton R.S., Williams B.J., Granholm A.C. Ovarian hormones and cognition in the aged female rat: II. progesterone supplementation reverses the cognitive enhancing effects of ovariectomy. Behav. Neurosci. 2004, 118:707-714.
15. Bimonte H.A., Denenberg V.H. Estradiol facilitates performance as working memory load increases. Psychoneuroendocrinology 1999, 24:161-173.
16. Bimonte H.A., Denenberg V.H. Sex differences in vicarious trial-and-error behavior during radial arm maze learning. Physiol. Behav. 2000, 68:495-499.
17. Bimonte H.A., Granholm A.C., Seo H., Isacson O. Spatial memory testing decreases hippocampal amyloid precursor protein in young, but not aged, female rats. Neurosci. Lett. 2002, 328:50-54.
18. Bimonte H.A., Hyde L.A., Hoplight B.J., Denenberg V.H. In two species, females exhibit superior working memory and inferior reference memory on the water radial-arm maze. Physiol. Behav. 2000, 70:311-317.
19. Bimonte H.A., Nelson M.E., Granholm A.C. Age-related deficits as working memory load increases: relationships with growth factors. Neurobiol. Aging 2003, 24:37-48.
20. Bowirrat A., Friedland R.P., Farrer L., Baldwin C., Korczyn A. Genetic and environmental risk factors for Alzheimer's disease in Israeli Arabs. J.Mol. Neurosci. 2002, 19:239-245.
21. Braden B.B., Talboom J.S., Crain I.D., Simard A.R., Lukas R.J., Prokai L., Scheldrup M.R., Bowman B.L., Bimonte-Nelson H.A. Medroxyprogesterone acetate impairs memory and alters the GABAergic system in aged surgically menopausal rats. Neurobiol. Learn. Mem. 2010, 93:444-453.
22. Braden B.B., Garcia A.N., Mennenga S.E., Prokai L., Villa S.R., Acosta J.I., Lefort N., Simard A.R., Bimonte-Nelson H.A. Cognitive-impairing effects of medroxyprogesterone acetate in the rat: independent and interactive effects across time. Psychopharmacology (Berl) 2011, 218:405-418.
23. Chiang K., Koo E.H. Emerging therapeutics for Alzheimer's disease. Annu. Rev. Pharmacol. Toxicol. 2014, 54:381-405.
24. Cohen J. Statistical Power Analysis for the Behavioral Sciences 1988, L. Erlbaum Associates, Hillsdale, NJ. second ed.
25. De Ronchi 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 socioeconomic status. Neurology 1998, 50:1231-1238.
26. Denenberg V.H., Sherman G.F., Schrott L.M., Rosen G.D., Galaburda A.M. Spatial learning, discrimination learning, paw preference and neocortical ectopias in two autoimmune strains of mice. Brain Res. 1991, 562:98-104.
27. Denenberg V.H., Talgo N.W., Schrott L.M., Kenner G.H. Acomputer-aided procedure for measuring discrimination learning. Physiol. Behav. 1990, 47:1031-1034.
28. Digby G.J., Noetzel M.J., Bubser M., Utley T.J., Walker A.G., Byun N.E., Lebois E.P., Xiang Z., Sheffler D.J., Cho H.P., Davis A.A., Nemirovsky N.E., Mennenga S.E., Camp B.W., Bimonte-Nelson H.A., Bode J., Italiano K., Morrison R., Daniels J.S., Niswender C.M., Olive M.F., Lindsley C.W., Jones C.K., Conn P.J. Novel allosteric agonists of M1 muscarinic acetylcholine receptors induce brain region-specific responses that correspond with behavioral effects in animal models. J.Neurosci. 2012, 32:8532-8544.
29. Drachman D.A., Leavitt J. Human memory and the cholinergic system. A relationship to aging?. Arch. Neurol. 1974, 30:113-121.
30. Eckerman D.A., Gordon W.A., Edwards J.D., MacPhail R.C., Gage M.I. Effects of scopolamine, pentobarbital, and amphetamine on radial arm maze performance in the rat. Pharmacol. Biochem. Behav. 1980, 12:595-602.
31. Engler-Chiurazzi E., Tsang C., Nonnenmacher S., Liang W.S., Corneveaux J.J., Prokai L., Huentelman M.J., Bimonte-Nelson H.A. Tonic Premarin dose-dependently enhances memory, affects neurotrophin protein levels and alters gene expression in middle-aged rats. Neurobiol. Aging 2011, 10.1016/j.neurobiolaging.2009.09.005.
32. Fischer W., Wictorin K., Bjorklund A., Williams L.R., Varon S., Gage F.H. Amelioration of cholinergic neuron atrophy and spatial memory impairment in aged rats by nerve growth factor. Nature 1987, 329:65-68.
33. Fitch R.H., Bimonte H.A. Hormones, brain, and behavior: putative biological contributions to cognitive sex differences. Biology, society, and behavior: the development of sex differences in cognition 2002, 55-91. Ablex Publishing Westport, CT. A.V. McGillicuddy-De Lisi, R., D.L. (Eds.).
34. Fritsch T., McClendon M.J., Smyth K.A., Ogrocki P.K. Effects of educational attainment and occupational status on cognitive and functional decline in persons with Alzheimer-type dementia. Int. Psychogeriatr. 2002, 14:347-363.
35. Gatz M., Svedberg P., Pedersen N.L., Mortimer J.A., Berg S., Johansson B. Education and the risk of Alzheimer's disease: findings from the study of dementia in Swedish twins. J.Gerontol. B Psychol. Sci. Soc. Sci. 2001, 56:P292-P300.
36. Gibbs R.B., Gabor R., Cox T., Johnson D.A. Effects of raloxifene and estradiol on hippocampal acetylcholine release and spatial learning in the rat. Psychoneuroendocrinology 2004, 29:741-748.
37. Goldman J.M., Murr A.S., Cooper R.L. The rodent estrous cycle: characterization of vaginal cytology and its utility in toxicological studies. Birth Defects Res. B Dev. Reprod. Toxicol. 2007, 80:84-97.
38. Goodman C.S., Shatz C.J. Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 1993, 72:77-98.
39. Granholm A.C. Oestrogen and nerve growth factor-neuroprotection and repair in Alzheimer's disease. Expert Opin. Investig. Drugs 2000, 9:685-694.
40. Gustilo M.C., Markowska A.L., Breckler S.J., Fleischman C.A., Price D.L., Koliatsos V.E. Evidence that nerve growth factor influences recent memory through structural changes in septohippocampal cholinergic neurons. J.Comp. Neurol. 1999, 405:491-507.
41. Hasselmo M.E. The role of acetylcholine in learning and memory. Curr. Opin. Neurobiol. 2006, 16:710-715.
42. Hebb D.O. The Organization of Behavior: A Neuropsychological Theory 1949, Wiley, New York.
43. Hyde L.A., Sherman G.F., Hoplight B.J., Denenberg V.H. Working memory deficits in BXSB mice with neocortical ectopias. Physiol. Behav. 2000, 70:1-5.
44. Ickes B.R., Pham T.M., Sanders L.A., Albeck D.S., Mohammed A.H., Granholm A.C. Long-term environmental enrichment leads to regional increases in neurotrophin levels in rat brain. Exp. Neurol. 2000, 164:45-52.
45. Jarrard L.E., Okaichi H., Steward O., Goldschmidt R.B. On the role of hippocampal connections in the performance of place and cue tasks: comparisons with damage to hippocampus. Behav. Neurosci. 1984, 98:946-954.
46. Juraska J.M. Sex differences in developmental plasticity of behavior and the brain. Developmental Neuropsychobiology 1986, 409-422. Academic Press, Inc., Orlando, FL. W.T. Greenough, J.M. Juraska (Eds.).
47. Keppel G., Wickens T.D. Design and Analysis: A Researcher's Handbook 2004, Pearson Prentice Hall, Upper Saddle River, NJ. fourth ed.
48. Koh S., Loy R. Age-related loss of nerve growth factor sensitivity in rat basal forebrain neurons. Brain Res. 1988, 440:396-401.
49. Lacreuse A., Kim C.B., Rosene D.L., Killiany R.J., Moss M.B., Moore T.L., Chennareddi L., Herndon J.G. Sex, age, and training modulate spatial memory in the rhesus monkey (Macaca mulatta). Behav. Neurosci 2005, 119:118-126.
50. Landau S.M., Marks S.M., Mormino E.C., Rabinovici G.D., Oh H., O'Neil J.P., Wilson R.S., Jagust W.J. Association of lifetime cognitive engagement andlow beta-amyloid deposition. Arch. Neurol 2012, 10.1001/archneurol.2011.2748.
51. Larkfors L., Ebendal T., Whittemore S.R., Persson H., Hoffer B., Olson L. Decreased level of nerve growth factor (NGF) and its messenger RNA in the aged rat brain. Brain Res. 1987, 427:55-60.
52. Letenneur L., Gilleron V., Commenges D., Helmer C., Orgogozo J.M., Dartigues J.F. Are sex and educational level independent predictors of dementia and Alzheimer's disease? Incidence data from the PAQUID project. J.Neurol. Neurosurg. Psychiatry 1999, 66:177-183.
53. Levi-Montalcini R. The nerve growth factor 35 years later. Science 1987, 237:1154-1162.
54. Light K.R., Kolata S., Wass C., Denman-Brice A., Zagalsky R., Matzel L.D. Working memory training promotes general cognitive abilities in genetically heterogeneous mice. Curr. Biol. 2010, 20:777-782.
55. Lindsay J., Laurin D., Verreault R., Hebert R., Helliwell B., Hill G.B., McDowell I. Risk factors for Alzheimer's disease: a prospective analysis from the Canadian Study of Health and Aging. Am. J. Epidemiol. 2002, 156:445-453.
56. Markowska A.L. Sex dimorphisms in the rate of age-related decline in spatial memory: relevance to alterations in the estrous cycle. J.Neurosci. 1999, 19:8122-8133.
57. Markowska A.L., Koliatsos V.E., Breckler S.J., Price D.L., Olton D.S. Human nerve growth factor improves spatial memory in aged but not in young rats. J.Neurosci. 1994, 14:4815-4824.
58. Markowska A.L., Price D., Koliatsos V.E. Selective effects of nerve growth factor on spatial recent memory as assessed by a delayed nonmatching-to-position task in the water maze. J.Neurosci. 1996, 16:3541-3548.
59. Markowska A.L., Savonenko A.V. Protective effect of practice on cognition during aging: implications for predictive characteristics of performance and efficacy of practice. Neurobiol. Learn. Mem. 2002, 78:294-320.
60. Matzel L.D., Light K.R., Wass C., Colas-Zelin D., Denman-Brice A., Waddel A.C., Kolata S. Longitudinal attentional engagement rescues mice from age-related cognitive declines and cognitive inflexibility. Learn Mem. 2011, 18:345-356.
61. Morris R.G., Garrud P., Rawlins J.N., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297:681-683.
62. Mufson E.J., Conner J.M., Kordower J.H. Nerve growth factor in Alzheimer's disease: defective retrograde transport to nucleus basalis. Neuroreport 1995, 6:1063-1066.
63. Guide for the Care and Use of Laboratory Animals 2011, National Research Council (U.S.) Committee for the Update of the Guide for the Care and Use of Laboratory Animals, Institute for Laboratory Animal Research (U.S.)Institute for Laboratory Animal Research (U.S.), National Academies Press (U.S.)National Academies Press (U.S.), National Academies Press, Washington, DC, xxv, 220 p.
64. Ott A., van Rossum C.T., van Harskamp F., van de Mheen H., Hofman A., Breteler M.M. Education and the incidence of dementia in a large population-based study: the Rotterdam Study. Neurology 1999, 52:663-666.
65. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 2005, Elsevier Academic Press, Amsterdam; Boston. fifth ed.
66. Petersen R.C., Stevens J.C., Ganguli M., Tangalos E.G., Cummings J.L., DeKosky S.T. Practice parameter: early detection of dementia: mild cognitive impairment (an evidence-based review). Report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology 2001, 56:1133-1142.
67. Pham T.M., Ickes B., Albeck D., Soderstrom S., Granholm A.C., Mohammed A.H. Changes in brain nerve growth factor levels and nerve growth factor receptors in rats exposed to environmental enrichment for one year. Neuroscience 1999, 94:279-286.
68. Rupniak N.M., Field M.J., Samson N.A., Steventon M.J., Iversen S.D. Direct comparison of cognitive facilitation by physostigmine and tetrahydroaminoacridine in two primate models. Neurobiol. Aging 1990, 11:609-613.
69. 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.
70. Shimamura A., Berry J., Mangels J., Rustig C. Memory and cognitive abilities in University professors. Psychol. Sci. 1995, 6:271-277.
71. Shrestha L.B. Life Expectancy in the United States 2005, Congressional Information Service, Library of Congress.
72. Siegel G.J., Chauhan N.B. Neurotrophic factors in Alzheimer's and Parkinson's disease brain. Brain Res. Brain Res. Rev. 2000, 33:199-227.
73. Singer J.D., Willett J.B. Applied longitudinal data analysis: modeling change and event occurrence 2003, Oxford University Press, Oxford; New York.
74. Snowdon D.A. Healthy aging and dementia: findings from the Nun Study. Ann. Intern. Med. 2003, 139:450-454.
75. Sugaya K., Greene R., Personett D., Robbins M., Kent C., Bryan D., Skiba E., Gallagher M., McKinney M. Septo-hippocampal cholinergic and neurotrophin markers in age-induced cognitive decline. Neurobiol. Aging 1998, 19:351-361.
76. Talboom J.S., Engler-Chiurazzi E.B., Whiteaker P., Simard A.R., Lukas R., Acosta J.I., Prokai L., Bimonte-Nelson H.A. Acomponent of Premarin(®) enhances multiple cognitive functions and influences nicotinic receptor expression. Horm. Behav. 2010, 58:917-928.
77. Vicens P., Carrasco M.C., Redolat R. Effects of early training and nicotine treatment on the performance of male NMRI mice in the water maze. Neural Plast. 2003, 10:303-317.
78. Vincent G.K., Velkoff V.A. The Next Four Decades: The Older Population in the United States: 2010 to 2050 2010, US Department of Commerce, Economics and Statistics Administration, US Census Bureau.
79. Warren S.G., Juraska J.M. Sex differences and estropausal phase effects on water maze performance in aged rats. Neurobiol. Learn. Mem. 2000, 74:229-240.
80. Whalley L.J., Starr J.M., Athawes R., Hunter D., Pattie A., Deary I.J. Childhood mental ability and dementia. Neurology 2000, 55:1455-1459.
81. Woolf N.J. Cholinergic systems in mammalian brain and spinal cord. Prog. Neurobiol. 1991, 37:475-524.