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Reproductive Experience may Positively Adjust the Trajectory of Senescence

  • Craig Howard KinsleyEmail author
  • R. Adam Franssen
  • Elizabeth Amory Meyer
Chapter
Part of the Current Topics in Behavioral Neurosciences book series (CTBN, volume 10)

Abstract

Although aging is inexorable, aging well is not. From the perspective of research in rats and complementary models, reproductive experience has significant effects; indeed, benefits, which include better-than-average cognitive skills, a slowing of the slope of decline, and a healthier brain and/or nervous system well later into life. Work from our lab and others has suggested that the events of pregnancy and parturition, collectively referred to as reproductive experience—an amalgam of hormone exposure, sensory stimulation, and offspring behavioral experience and interaction—may summate to flatten the degree of decline normally associated with aging. Mimicking the effects of an enriched environment, reproductive experience has been shown to: enhance/protect cognition and decrease anxiety well out to two-plus years; result in fewer hippocampal deposits of the Alzheimer’s disease herald, amyloid precursor protein (APP); and, in general, lead to a healthier biology. Based on a suite of recent work in organisms as diverse as nematodes, flies, and mammals, the ubiquitous hormone insulin and its large family of related substances and receptors may play a major role in mediating some of the effects of RE on the parameters of aging studied thus far. We will discuss the current set of data that suggest mechanisms for successful biological and neurobiological aging, and the implications for understanding aging and senescence in their broadest terms.

Keywords

Amyloid precursor protein (APP) Enriched environment Hippocampus  Lactation  Learning and memory Medial preoptic area Oxytocin Parity effects  Pregnancy  Reproductive experience Senescence Steroid hormones 

References

  1. Agaram R, Douglas MJ, McTaggart RA, Gunka V (2009) Inadequate pain relief with labor epidurals: a multivariate analysis of associated factors. Int J Obstet Anesth 18:10–14PubMedCrossRefGoogle Scholar
  2. Ahima RS, Flier JS (2000) Adipose tissue as an endocrine organ. Trends in Endocrinol Metlab 11:327–332CrossRefGoogle Scholar
  3. Altman J, Das GD (1965) Post-natal origin of microneurons in the rat brain. Nature 207:953–956PubMedCrossRefGoogle Scholar
  4. Anisimov VN et al (2008) Metformin slows down aging and extends life span of female SHR mice. Cell Cycle 7:2769–2773PubMedCrossRefGoogle Scholar
  5. Apfeld J, O’Connor G, McDonagh T, DiStefano PS, Curtis R (2004) The AMP-activated protein kinase AAK-2 links energy levels and insulin-like signals to lifespan in C. elegans. Genes Dev 18:3004–3009PubMedCrossRefGoogle Scholar
  6. Auger CJ, De Vries GJ (2002) Distribution and steroid responsiveness of progestin receptor immunoreactivity within vasopressin-immunoreactive cells in the bed nucleus of the stria terminalis and the centromedial amygdala of male and female rat brain. J Neuroendocrinol 14:161–167Google Scholar
  7. Azcoitia I, DonCarlos LL, Garcia-Segura LM (2003) Are gonadal steroid hormones involved in disorders of brain aging? Aging Cell 2:31–37PubMedCrossRefGoogle Scholar
  8. Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, Kalra A, Prabhu VV, Allard JS, Lopez-Lluch G, Lewis K, Pistell PJ, Poosala S, Becker KG, Boss O, Gwinn D, Wang M, Ramaswamy S, Fishbein KW, Spencer RG, Lakatta EG, Le Couteur D, Shaw RJ, Navas P, Puigserver P, Ingram DK, de Cabo R, Sinclair DA (2006) Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444:337–342PubMedCrossRefGoogle Scholar
  9. Beevers C, Li F, Liu L, Huang S (2006) Curcumin inhibits the mammalian target of rapamycin-mediated signaling pathways in cancer cells. Int J Cancer 119:757–764PubMedCrossRefGoogle Scholar
  10. Behl C, Widmann M, Trapp T, Holsboer F (1995) 17-β Estradiol Protects Neurons from Oxidative Stress-Induced Cell Death in Vitro. Biochem Biophys Res Comm 216:473–482PubMedCrossRefGoogle Scholar
  11. Bennett DA, Wilson RS, Schneider JA, Evans DA, Mendes De Leon CF, Arnold SE, Barnes LL, Bienias JL (2003) Education modifies the relation of AD pathology to level of cognitive function in older persons. Neurology 60:1909–1915PubMedCrossRefGoogle Scholar
  12. Bishop NA, Lu T, Yankner BA (2010) Neural mechanisms of ageing and cognitive decline. Nature 464:529–535PubMedCrossRefGoogle Scholar
  13. Bluher M, Peroni OD, Ueki K, Carter N, Kahn BB, Kahn CR (2002) Adipose tissue selective insulin receptor knockout protects against obesity and obesity-related glucose intolerance. Dev. Cell 3:25–38PubMedCrossRefGoogle Scholar
  14. Bluher M, Khan BP, Kahn CR (2003) Extended longevity in mice lacking the insulin receptor in adipose tissue. Science 299:572–574PubMedCrossRefGoogle Scholar
  15. Bridges RS (1975) Long-term effects of pregnancy and parturition upon maternal responsiveness in the rat. Physiol Behav 14:245–249PubMedCrossRefGoogle Scholar
  16. Bridges RS, Grimm CT (1982) Reversal of morphine disruption of maternal behavior by concurrent treatment with the opiate antagonist naloxone. Science 218:166–168PubMedCrossRefGoogle Scholar
  17. Bridges RS (1984) A quantitative analysis of the roles of dosage, sequence, and duration of estradiol and progesterone exposure in the regulation of maternal behavior in the rat. Endocrinology 114:930–940PubMedCrossRefGoogle Scholar
  18. Bridges RS (1990) Endocrine regulation of parental behavior in rodents. In: Krasnegor NA, Bridges RS (eds) Mammalian Parenting: Biochemical, Neurobiological and Behavioral Determinants. Oxford University Press, New York, pp 93–117Google Scholar
  19. Bridges RS, Hammer Jr RP (1992) Parity-associated alterations in medial preoptic opiate receptors in female rats. Brain Res 578:269–274PubMedCrossRefGoogle Scholar
  20. Bridges RS, Felicio LF, Pellerin LJ, Steuer AM, Mann PE (1993) Prior parity reduces post-coital diurnal and nocturnal prolactin surges in rats. Life Sci 53:439–445PubMedCrossRefGoogle Scholar
  21. Bridges RS, Robertson MC, Shiu RPC, Friesen HG, Stuer AM, Mann PE (1996) Endocrine communication between conceptus and mother: a role for placental lactogens in the induction of maternal behavior. Neuroendocrinology 64:57–64PubMedCrossRefGoogle Scholar
  22. Bridges RS, Robertson MC, Shiu RP, Sturgis JD, Henriquez BM, Mann PE (1997) Central lactogenic regulation of maternal behavior in rats: steroid dependence, hormone specificity, and behavioral potencies of rat prolactin and rat placental lactogen. Endocrinol 138:756–763CrossRefGoogle Scholar
  23. Bridges RS (2009) The Neurobiology of the Parental Brain. Academic Press, New YorkGoogle Scholar
  24. Broue F, Liere P, Kenyon C, Baulieu EE (2007) A steroid hormone that extends the lifespan of Caenorhabditis elegans. Aging Cell 6:87–94PubMedCrossRefGoogle Scholar
  25. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96:857–868PubMedCrossRefGoogle Scholar
  26. Brunet A, Sweeney LB, Sturgill JF, Chua KF, Greer PL, Lin Y, Tran H, Ross SE, Mostoslavsky R, Cohen HY, Hu LS, Cheng H, Jedrychowski MP, Gygi SP, Sinclair DA, Alt FW, Greenberg ME (2004) Stress-Dependent Regulation of FOXO Transcription Factors by the SIRT1 Deacetylase. Science 303:2011–2015PubMedCrossRefGoogle Scholar
  27. Cameron HA, Gould E (1994) Adult neurogenesis is regulated by adrenal steroids in the rat dentate gyrus. Neuroscience 61:203–209PubMedCrossRefGoogle Scholar
  28. Carlen M, Cassidy RM, Brismar H, Smith GA, Enquist LW, Freisen J (2002) Functional integration of adult-born neurons. Curr Biol 12:606–608PubMedCrossRefGoogle Scholar
  29. Carleton A, Petreanu LT, Lansford R, Alvarez-Buylla A, Lledo PM (2003) Becoming a new neuron in the adult olfactory bulb. Nat Neurosci 6:507–518PubMedGoogle Scholar
  30. Carro E, Nunez A, Busiguina S, Torres-Aleman I (2001) Circulating insulin-like growth factorI mediates effects of exercise on the brain. J Neurosci 20:2926–2933Google Scholar
  31. Colman RJ et al (2009) Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 325:201–204PubMedCrossRefGoogle Scholar
  32. Conover CA, Bale LK (2007) Loss of pregnancy-associated plasma protein A extends lifespan in mice. Aging Cell 6:727–729PubMedCrossRefGoogle Scholar
  33. Contino R, Friedenberg J, Christon L, Norkunas T, Worthington D, Jablow L, Drew M, Victoria L, Chipko C, Sirkin M, Ferguson T, Jones C, Bardi M, Lambert KG and Kinsley CH (2007). The expression of the maternal Brain: Specific genes involved in the neuroplasticity of motherhood. Paper presented at the Society for Neuroscience annual meeting, San Diego, CA, NovemberGoogle Scholar
  34. Coschigano KT, Holland AN, Riders ME, List EO, Flyvbjerg A, Kopchick JJ (2003) Deletion, but not antagonism, of the mouse growth hormone receptor results in severely decreased body weights, insulin, and insulin-like growth factor I levels and increased life span. Endocrinology 144:3799–3810PubMedCrossRefGoogle Scholar
  35. Cummins RA, Walsh RN, Budtz-Olsen OE, Konstantinos, Horsfall CR (1973) Environmentally induced changes in the brains of elderly rats. Nature 243:516–518Google Scholar
  36. Cummins RA, Livesey PJ, Evans JG (1977) A developmental theory of environmental enrichment. Science 197:692–694PubMedCrossRefGoogle Scholar
  37. Dagyte G, Trentani A, Postema F, Luiten PG, Den Boaer JA, Gabriel C, Mocaer E, Meerlo P, Van de Zee EA (2010) The novel antidepressant agomelatine normalizes hippocampal neuronal activity and promotes neurogenesis in chronically stressed rats. CNS Neurosci Ther 16:195–207PubMedCrossRefGoogle Scholar
  38. Diamond MC, Krech D, Rosenzweig MR (1964) The effects of an enriched environment on the histology of the rat cerebral cortex. J Comp Neurol 123:111–120PubMedCrossRefGoogle Scholar
  39. Diamond MC, Johnson RE, Ingham C (1971) Brain plasticity induced by environment and pregnancy. Int J Neurosci 2:171–178PubMedCrossRefGoogle Scholar
  40. Doonan R, Mcelwee JJ, Matthijssens F, Walker GA, Houthood K, Back P, Matscheski A, Vanfleteren JR, Gems D (2008) Against the oxidative damage theory of aging: superoxide dismutases protect against oxidative stress but have little or no effect on life span in Caenorhabditis elegans. Genes Dev 22:3226–3241Google Scholar
  41. Enwere E, Shingo T, Gregg C, Fujikawa H, Ohta O, Weiss S (2004) Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J Neurosci 24:8354–8365PubMedCrossRefGoogle Scholar
  42. Fabrizio P, Pozza F, Pletcher SD, Gendron CM, Longo VD (2001) Regulation of longevity and stress resistance by Sch9 in yeast. Science 292:288–290PubMedCrossRefGoogle Scholar
  43. Fabrizio P, Liou LL, Moy VN, Diaspro A, Valentine JS, Gralla EB, Longo VD (2003) SOD2 functions downstream of Sch9 to extend longevity in yeast. Genetics 163:35–46PubMedGoogle Scholar
  44. Feige JN, Lagouge M, Canto C, Strehle A, Houten SM, Milne JC, Lambert PD, Mataki PJ, Auwerx J (2008) Specific SIRT1 activation mimics low energy levels and protects against diet-induced metabolic disorders by enhancing fat oxidation. Cell Met 8:347–358CrossRefGoogle Scholar
  45. Felicio LF, Florio JC, Sider LH, Cruz-Casallas PE, Bridges RS (1996) Reproductive experience increases striatal and hypothalamic dopamine levels in pregnant rats. Brain Res Bull 40:253–256CrossRefGoogle Scholar
  46. Fischer A, Sananbenesi F, Wang X, Dobbin M, Tsai LH (2007) Recovery of learning and memory is associated with chromatin remodeling. Nature 447:178–182PubMedCrossRefGoogle Scholar
  47. Flint DJ, Sinnett-Smith PA, Clegg RA, Vernon RG (1979) Role of insulin receptors in the changing metabolism of adipose tissue during pregnancy and lactation in the rat. Biochem J 182:421–427PubMedGoogle Scholar
  48. Flurkey K, Papaconstantinou J, Miller RA, Harrison DE (2001) Lifespan extension and delayed immune and collagen aging in mutant mice with defects in growth hormone production. Proc Natl Acad Sci 98:6736–6741PubMedCrossRefGoogle Scholar
  49. Fontana L, Klein S (2007) Aging, adiposity and calorie restriction. JAMA 297:986–994PubMedCrossRefGoogle Scholar
  50. Fontana L, Partridge L, Longo VD (2010) Extending healthy life span from yeasts to humans. Science 328:321–326PubMedCrossRefGoogle Scholar
  51. Frescas D, Valenti L, Accili D (2005) Nuclear trapping of the forkhead transcription factor FoxO1 via sirt-dependent deacetylation promotes expression of glucogenetic genes. J Biol Chem 280:20589–20595PubMedCrossRefGoogle Scholar
  52. Furuta M, Bridges RS (2005) Gestation-induced cell proliferation in the rat brain. Brain Res Dev Brain Res 156:61–66PubMedCrossRefGoogle Scholar
  53. Gatewood JD, Morgan MD, Eaton M, McNamara IM, Stevens LF, Macbeth AH, Meyers EAA, Lomas LM, Kozub FJ, Lambert KG, Kinsley CH (2005) Motherhood mitigates aging-related decrements in learning and memory. Brain Res Bull 59:267–283Google Scholar
  54. Ge H, Wei M, Fabrizio P, Hu J, Cheng C, Longo VD, Li LM (2010) Comparative analyses of time-course gene expression profiles of the long-lived sch9Δ mutant. Nucl Acids Res 38:143–158PubMedCrossRefGoogle Scholar
  55. Gould E, Cameron HA, Daniels DC, Woolley CS, McEwen BS (1992) Adrenal hormones suppress cell division in the adult rat dentate gyrus. J Neurosci 12:3642–3650PubMedGoogle Scholar
  56. Gould E, McEwan BS, Tanapat P, Galea LA, Fuchs E (1997) Neurogenesis in the dentate gyrus of the adult tree shrew is reguilated by psychosocial stress and NMDA receptor activation. J Neurosci 17:2492–2498PubMedGoogle Scholar
  57. Gould E, Tanapat P, Hastings NB, Shors TJ (1998) Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci 95:3168–3171PubMedCrossRefGoogle Scholar
  58. Greer EL, Brunet A (2010) Signaling networks in aging. J Cell Sci 121:407–412CrossRefGoogle Scholar
  59. Gruber J, Tang SY, Halliwell B (2007) Evidence for a trade-off between survival and fitness caused by resveratrol treatment of Caenorhabditis elegans. Ann NY Acad Sci 1100:530–542PubMedCrossRefGoogle Scholar
  60. Guerra-Araiza C, Reyna-Neyra A, Salazar AM, Cerbon MA, Morimoto S, Camacho-Arroyo I (2001) Progesterone receptor isoforms expression in the prepuberal and adult male rat brain. Brain Res Bull 54:13–17PubMedCrossRefGoogle Scholar
  61. Gursoy E, Cardounel A, Kalimi M (2001) Pregnenolone protects mouse hippocampal (HT-22) cells against glutamate and amyloid beta protein toxicity. Neurochem Res 26:15–21PubMedCrossRefGoogle Scholar
  62. Halagappa VK et al (2007) Intermittent fasting and caloric restriction ameliorate age-related behavioral deficits in the triple-transgenic mouse model of Alzheimer’s disease. Neurobiol Dis 26:212–220PubMedCrossRefGoogle Scholar
  63. Hara T et al (2006) Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441:885–889PubMedCrossRefGoogle Scholar
  64. Harrison DE et al (2009) Rapamycin fed late in life extends lifespan in genetically heterogenous mice. Nature 460:392–395PubMedGoogle Scholar
  65. Hatton GI, Zhao Yang Q (2002) Peripartum interneuronal coupling in the supraoptic nucleus. Brain Res 932:120–123PubMedCrossRefGoogle Scholar
  66. Hay N, Sonenberg N (2004) Upstream and downstream of mTOR. Genes Dev 18:1926–1945PubMedCrossRefGoogle Scholar
  67. Henderson ST, Johnson TE (2001) DAF-16 integrates developmental and environmental inputs to mediat aging in the nematode Caenorhabditis elegans. Curr Biol 11:1975–1980PubMedCrossRefGoogle Scholar
  68. Holliday R (2005) Food, reproduction and longevity: is the extended lifespan of calorie-restricted animals an evolutionary adaptation? Bioessays 10:125–127CrossRefGoogle Scholar
  69. Howitz KT, Bitterman KJ, Cohen HY, Lamming DW, Lavu S, Wood JG, Zipkin RE, Chung P, Kisielewski A, Zhang LL, Scherer B, Sinclair DA (2003) Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 425:191–196PubMedCrossRefGoogle Scholar
  70. Hsin H, Kenyon C (1999) Signals from the reproductive system regulate the lifespan of C. elegans. Nature 399:362–366PubMedCrossRefGoogle Scholar
  71. Hwangbo DS, Gersham B, Tu MP, Palmer M, Tatar M (2004) Drosophila dFOXO controls lifespan and regulates insulin signaling in brain and fat body. Nature 492:562–566CrossRefGoogle Scholar
  72. Johnson TE (2008) Caenorhabditis elegans. (2007). The premier model for the study of aging. Exp Gerontol 43:1–4PubMedCrossRefGoogle Scholar
  73. Kaeberlein M, Powers III RW, Steffen KK, Westman EA, Hu D, Dang N, Kerr EO, Kirkland KT, Fields S, Kennedy BK (2005) Regulation of yeast replicative life span by TOR and Sch9 in response to nutrients. Science 310:1193–1196PubMedCrossRefGoogle Scholar
  74. Kapahi P, Zid BM, Harper T, Koslover D, Sapin V, Benzer S (2004) Regulation of lifespan in Drosophila by modulation of genes in the TOR signaling pathway. Curr Biol 14:885PubMedCrossRefGoogle Scholar
  75. Kempermann G (2006) Adult neurogenesis. Oxford, Oxford PressGoogle Scholar
  76. Kempermann G, Gage F (1998) Closer to neurogenesis in adult humans. Nat Med 4:555–557PubMedCrossRefGoogle Scholar
  77. Kempermann G, Kuhn G, Gage F (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386:493–495PubMedCrossRefGoogle Scholar
  78. Kempermann G, Brandon EP, Gage F (1998) Environmental stimulation of 129/SvJ mice causes increased cell proliferation and neurogenesis in the adult dentate gyrus. Curr Biol 8:939–942PubMedCrossRefGoogle Scholar
  79. Kempermann G, Gast D, Gage F (2002) Neuroplasticity in old age:sustained five-fold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann Neurol 52:135–143PubMedCrossRefGoogle Scholar
  80. Kenyon CJ (2010) The genetics of ageing. Nature 464:504–512PubMedCrossRefGoogle Scholar
  81. Kesner R, Dakis M (1995) Phencyclidine injections into the dorsal hippocampus disrupt long-but not short-term memory within a spatial learning task. Psychopharmacology 120:203–208PubMedCrossRefGoogle Scholar
  82. Keyser L, Stafisso-Sandoz G, Gerecke K, Jasnow A, Nightingale L, Lambert KG, Gatewood J, Kinsley CH (2001) Alterations of medial preoptic area neurons following pregnancy and pregnancy-like steroidal treatment in the rat. Brain Res Bull 55:737–745CrossRefGoogle Scholar
  83. Kinsley CH, Bridges RS (1988) Parity associated reductions in behavioral sensitivity to opiates. Biol Reprod 39:270–278PubMedCrossRefGoogle Scholar
  84. Kinsley CH (1994) Developmental psychobiological influences on rodent parental behavior. Neurosci Biobehav Rev 18:269–280PubMedCrossRefGoogle Scholar
  85. Kinsley CH, Madonia L, Gifford GW, Tureski K, Griffin GR, Lowry C, Williams J, Collins J, McLearie H, Lambert KG (1999) Motherhood improves learning and memory: Neural activity in rats is enhanced by pregnancy and the demands of rearing offspring. Nature 402:137–138PubMedCrossRefGoogle Scholar
  86. Kinsley CH, Lambert KG, The Maternal Brain (2006) Pregnancy and motherhood change the structure of the female mammal’s brain, making mothers attentive to their young and better at caring for them. Scientific American January 2006Google Scholar
  87. Kinsley CH, Trainer R, Stafisso-Sandoz G, Quadros P, Keyser-Marcus L, Hearon C, Wightman N, Morgan MD, Kozub FJ, Lambert KG (2006) Motherhood and pregnancy hormones modify concentrations of hippocampal neuronal dendritic spines. Horm Behav 49:131–142PubMedCrossRefGoogle Scholar
  88. Kinsley CH (2008) The neuroplastic maternal brain. Horm Behav 54:1–4PubMedCrossRefGoogle Scholar
  89. Kinsley CH, Lambert KG (2008) Reproduction-induced neuroplasticity: natural behavioral and neuronal alterations associated with the production and care of offspring. J Neuroendocrinology 20:515–525CrossRefGoogle Scholar
  90. Kinsley CH, Bardi M, Karelina K, Rima B, Christon L, Friedenberg J, Griffin G (2008) Motherhood Induces and Maintains Behavioral and Neural Plasticity Across the Lifespan in the Rat. Arch of Sex Behav 37:43–56Google Scholar
  91. Klionsky DJ, Emr SD (2000) Autophagy as a regulated pathway of cellular degradation. Science 290:1717–1721PubMedCrossRefGoogle Scholar
  92. Koenig HL, Schumacher M, Ferzaz B, Thi AN, Ressouches A, Guennoun R, Jung-Testas I, Robel P, Akwa Y, Baulieu EE (1995) Progesterone synthesis and myelin formation by Schwann cells. Science 268:1500–1503PubMedCrossRefGoogle Scholar
  93. Kozorovitskiy Y, Hughes M, Lee K, Gould E (2006) Fatherhood affects dendritic spines and vasopressin V1a receptors in the primate prefrontal cortex. Nat Neurosci 9:1094–1095PubMedCrossRefGoogle Scholar
  94. Kumangai S, Holmang A, Bjorntorp P (1993) The effects of oestrogen and progesterone on insulin sensitivity in female rats. Acta Phys Scand 149:91–97CrossRefGoogle Scholar
  95. Kuro-o M (2009) Klotho and aging. Biochem Biophys Acta 1790:1049–1058PubMedCrossRefGoogle Scholar
  96. Kuro-o M, Matsumura Y, Aizawa H, Kawaguchi H, Suga T, Utsugi T, Ohyama Y, Kurabayashi M, Kaname T, Kume E, Iwasaki H, Iida A, Shiraki-Iida T, Nishikawa S, Nagai R, Nabeshima YI (1997) Mutation of the mouse klotho gene leads to a syndrome resembling ageing. Nature 390:45–51PubMedCrossRefGoogle Scholar
  97. Kuroshu H, Yamamoto M, Clark JD, Pastor JV, Nandi A et al (2005) Suppression of aging in mice by the hormone Klotho. Science 309:1829–1833CrossRefGoogle Scholar
  98. Lambert KG, Kinsley CH (2009) The neuroeconomics of motherhood: the costs and benefits of maternal investment. In Bridges RS (ed.), The Neurobiology of the Parental Brain. 481–492, Academic PressGoogle Scholar
  99. Lambert KG, Berry AE, Griffin G, Amory-Meyer EA, Madonia-Lomas LF, Love G, Kinsley CH (2005) Pup exposure differentially enhances foraging ability in primiparous and nulliparous rats. Physiol Behav 85:799–806CrossRefGoogle Scholar
  100. Lichtenwalner RJ, Forbes ME, Bennett SA, Lynch CD, Sonntag WE, Riddle DR (2001) Intracerebroventricular infusion of insulin-like growth factor-I ameliorates the age related decline in hippocampal neurogenesis. Neuroscience 107:603–613PubMedCrossRefGoogle Scholar
  101. Liu Y, Neve RL, Taylor P, Driscoll M, Clardy J, Merry D, Kalb RG (2004) FOXO3a is broadly neuroprotective in vitro and in vivo against insults implicated in motor neuron diseases. J Neurosci 29:8236–8247Google Scholar
  102. Love G, Torrey N, McNamara I, Morgan M, Banks M, Wightman N, Glasper ER, DeVries AC, Kinsley CH, Lambert KG (2005) Maternal experience produces long lasting behavioral modifications in the rat. Behav Neurosci 119:1084–1096PubMedCrossRefGoogle Scholar
  103. Lucking R, Huhndorf S, Pfister D, Plata ER, Lumbsch H (2009) Fungi evolved right on track. Mycologia 101:810–822PubMedCrossRefGoogle Scholar
  104. Mak HY, Ruvkun G (2004) Intercellular signaling of reproductive development by the C. elegans DAF-9 cytochrome P450. Development 131:1777–1786PubMedCrossRefGoogle Scholar
  105. Mak GK, Weiss S (2010) Paternal recognition of adult offspring mediated by newly generated CNS neurons. Nat Neurosci 13:753–758PubMedCrossRefGoogle Scholar
  106. Mann PE, Bridges RS (1992) Neural and endocrine sensitivities decline as a function of multiparity in the rat. Brain Res 580:241–248PubMedCrossRefGoogle Scholar
  107. Maroso EJ (2005) Overview of caloric restriction and ageing. Mech Ageing Dev 126:913–922CrossRefGoogle Scholar
  108. Maviel T, Durkin TP, Menzaghi F, Bontempi B (2004) Sites of cortical reorganization critical for remote spatial memory. Science 305:96–99PubMedCrossRefGoogle Scholar
  109. McEwen BS, Woolley CS (1994) Estradiol and progesterone regulate neuronal structure and synaptic connectivity in adult as well as developing brain. Exp Gerontol 29:431–436PubMedCrossRefGoogle Scholar
  110. Melendez A et al (2003) Autophagy genes are essential to dauer development and life-span extension in C elegans. Science 301:1387–1391PubMedCrossRefGoogle Scholar
  111. Messines IE, Papageorgiou I, Milingo S, Asprodini E, Kollios G, Seferiadis K (2001) Oestradiol plus progesterone treatment increases serum leptin concentrations in normal women. Hum Repro 16:1827–1832CrossRefGoogle Scholar
  112. Miller S, Erskine MS (1995) Ultrastructural effects of estradiol and 5-alpha-androstane on neurons within the ventromedial nucleus of the hypothalamus. Neuroendocrinology 61:669–679PubMedCrossRefGoogle Scholar
  113. Modney BK, Hatton GI (1994) Maternal behaviors: evidence that they feed back to alter brain morphology and function. Acta Paediatr 83:29–32CrossRefGoogle Scholar
  114. Mojsilovic-Petrovic J, Nedelsky N, Boccitto M, Mano I, Georgiades SN, Zhou W, Liu Y, Neve RL, Taylor PJ, Driscoll M, Clardy J, Merry D, Kalb RG (2009) FOXO3a is broadly neuroprotective in vitro and in vivo against insults implicated in motor neuron diseases. J Neuro 29:8236–8247CrossRefGoogle Scholar
  115. Moltz H, Levin R, Leon M (1969) Differential effects of progesterone on the maternal behavior of primiparous and multiparous rats. J Comp Physiol Psychol 67:36–40PubMedCrossRefGoogle Scholar
  116. Mostoslavsky R, Chua KF, Lombard DB, Pang WW et al. (2006) Genomic instability and aging-like phenotype in the absence of mammalian SIRT6. Cell 124:315–329PubMedCrossRefGoogle Scholar
  117. Muller FL, Lustgarten MS, Jang Y, Richardson A, Van Remmen H (2007) Trends in oxidative aging theories. Free Radic Biol Med 43:477–503PubMedCrossRefGoogle Scholar
  118. Murakami K, Fellous A, Baulieu E, Robel P (2000) Pregnenolone binds to microtubule-associated protein 2 and stimulates microtubule assembly PNAS 97:3579–3584Google Scholar
  119. Nilsson M, Perfilieva E, Johansson U, Orwar O, Erikccon PS (1999) Enriched environment increases neurogenesis in the adult rat and improves spatial memory. J Neurobiol 39:569–578PubMedCrossRefGoogle Scholar
  120. Numan M, Insel TR (2003) The neurobiology of parental behavior. Springer-Verlag, New YorkGoogle Scholar
  121. Olshansky JS, Passaro DJ, Hershow RC, Layden J, Carnes BA, Brody J, Hayflick L, Butler RN, Allison DB, Ludwig DS (2005) A potential deline in life expectancy in the United States in the twenty-first century. N Engl J Med 352:1138–1145PubMedCrossRefGoogle Scholar
  122. Pan Y, Shadel GS (2009) Extension of chronological life span by reduced TOR signaling requires down-regulation of Sch9p and involves increased mitochondrial OXPHOS complex density. Aging 1:131–145PubMedGoogle Scholar
  123. Pascual-Leone A, Amedi A, Fregni F, Merabet LB (2005) The plastic human brain cortex. Ann Rev Neuroscience 28:377–401CrossRefGoogle Scholar
  124. Pettorelli N, Durant SM (2007) Longevity in cheetahs: the key to success? Oikos 116:1879–1886CrossRefGoogle Scholar
  125. Phelan JP, Rose MR (2005) Why dietary restriction substantially increases longevity in animal models but won’t work in humans. Age Res Rev 4:339–350CrossRefGoogle Scholar
  126. Radak Z, Hart N, Sarga L, Koltai E, Atalay M, Ohno H, Boldogh I (2010) Exercise plays a preventative role against Alzheimer’s disease. J Alzheimers Dis 20:777–783PubMedGoogle Scholar
  127. Rehm S, Deerberg F, Rapp KG (1984) A comparison of life-span and spontaneous tumor incidence of male and female Han: WIST Virginia and retired breeders. Lab Anim Sci 34:458–464PubMedGoogle Scholar
  128. Rose G, Dato S, Altomare K, Bellizzi D, Garasto S, Greco V, Passarino G, Feraco E, Mari V, Barbi C, Bonafe M, Franceschi C, Tan Q, Boiko S, Yashin, AI, De Benedictis G (2003) Variability of the SIRT3 gene, human silent information regulator Sir2 homologue, and survivorship in the elderly. Exp Gerontol 38:1065–1070PubMedCrossRefGoogle Scholar
  129. Russel SJ, Kahn CR (2007) Endocrine regulation of ageing. Nat Rev Mol Cell Biol 8:681–691CrossRefGoogle Scholar
  130. Schumacher M, Weill-Engerer S, Liere P, Robert F, Franklin RJM, Garcia-Segura LM, Lambert JJ, Mayo W, Melcangi RC, Parducz A, Suter U, Carelli C, Baulieu EE, Akwa Y (2003) Steroid hormones and neurosteroids in normal and pathological aging of the nervous system. Prog Neurobiol 71:3–29PubMedCrossRefGoogle Scholar
  131. Selman C, Tullet JM, Wieser D, Irvine E, Lingard SJ, Choudhury AI, Claret M, Al-Qassab H, Carmignac D, Ramadani F, Woods A, Robinson IC, Schuster E, Batterham RL, Kozma SC, Thomas G, Carling D, Okkenhaug K, Thornton JM, Partridge L, Gems D, Withers DJ (2009) Ribosomal Protein S6 Kinase 1 Signaling Regulates Mammalian Life Span. Science 326:140–144PubMedCrossRefGoogle Scholar
  132. Shingo T, Gregg C, Enwere E, Fujikawa H, Hassam R, Geary C, Cross JC, Weiss S (2003) Pregnancy stimulated neurogenesis in the adult female forebrain is mediated by prolactin. Science 299:117–120PubMedCrossRefGoogle Scholar
  133. Simon AF, Shih C, Mack A, Benzer S (2003) Steroid control of longevity in Drosophila melanogaster. Science 299:1407–1410PubMedCrossRefGoogle Scholar
  134. Simonsen A et al (2008) Promoting basal levels of autophagy in the nervous system enhances longevity and oxidant resistence in adult Drosophila. Autophagy 4:176–184PubMedGoogle Scholar
  135. Stern JM (1996) Somatosensation and maternal care in Norway Rats. In: Rosenblatt JS, Snowden CT (eds) Parental care: Evolution, mechanisms, and adaptive significance. Academic Press, New York, NYGoogle Scholar
  136. Suzuki S, Gerhold LM, Böttner M, Rau SW, Dela Cruz C, Yang E, Zhu H, Yu J, Cashion AB, Kindy MS, Merchenthaler I, Gage FH, Wise PM (2001) Estradiol enhances neurogenesis following ischemic stroke through estrogen receptors alpha and beta. J Comp Neurol 6:1064–1075Google Scholar
  137. Svare B, Gandelman R (1976) A longitudinal analysis of maternal aggression in Rockland-Swiss albino mice. Dev Psychobiol 9:437–446PubMedCrossRefGoogle Scholar
  138. Tanapat P, Hastings NB, Reeves AJ, Gould E (1999) Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci 19:5792–5801PubMedGoogle Scholar
  139. Thomas F, Teriokhin AT, Budilova EV, Brown SP, Renaud F, Guegan JF (2000) Human longevity at the cost of reproductive success: evidence from global data. J Evo Biol 13:409–414CrossRefGoogle Scholar
  140. Tissenbaum HA, Guarente L (2001) Increased dosage of a sir-2 gene extends lifespan in Caenorhabditis elegans. Nature 410:227–230PubMedCrossRefGoogle Scholar
  141. Tomizawa K, Iga N, Lu Y-F, Moriwaki A, Matsushita M, Li S-T, Miyamato O, Itano T, Matsui H (2003) Oxytocin improves long-lasting spatial memory during motherhood through MAP kinase cascade. Nat Neurosci 6:384–390PubMedCrossRefGoogle Scholar
  142. Toth AL, Varala K, Newman TC, Miguez FE, Hutchison SK, Willoughby DA, Simons JF, Egholm M, Hunt JH, Hudson ME, Robinson GE (2007) Wasp gene expression supports an evolutionary link between maternal behavior and eusociality. Science 318:441–444PubMedCrossRefGoogle Scholar
  143. Valenzano DR, Terzibasi E, Genade T, Cattaneo A, Domenici L, Cellerino A (2006) Resveratrol prolongs lifespan and retards the onset of age-related markers in a short-lived vertebrate. Curr Biol 16:296–300PubMedCrossRefGoogle Scholar
  144. Vallée M, Mayo W, Le Moal M (2001) Role of pregnenolone, hydroepiandrosterone and their sulfate esters on learning and memory in cognitive aging. Brain Res Brain Res Rev 37:301–312PubMedCrossRefGoogle Scholar
  145. Van der Heide LP, Ramakers GM, Smidt MP (2006) Insulin signaling in the central nervous system: learning to survive. Prog Neurobiol 79:205–221PubMedCrossRefGoogle Scholar
  146. Van Praag H, Christie B, Sejnowski TJ, Gage F (1999) Running enhances neurogenesis, learning and long-term potentiation in mice. Proc Natl Acad Sci 96:13427–13431PubMedCrossRefGoogle Scholar
  147. Viswanathan M, Kim SK, Berdichevsky A, Guarente L (2005) A Role for SIR-2.1 regulation of ER stress response genes in determining C. elegans life span. Dev Cell 9:605–615PubMedCrossRefGoogle Scholar
  148. Volkmar FR, Greenough WT (1972) Rearing complexity affects branching of dendrites in the visual cortex of the rat. Science 176:1145–1147CrossRefGoogle Scholar
  149. Wartella J, Amory E, Madonia-Lomas L, Macbeth AH, McNamara I, Stevens L, Lambert KG, Kinsley CH (2003) Single or multiple reproductive experiences attenuate neurobehavioral stress and fear responses in the female rat. Physiol Behav 79:373–381PubMedCrossRefGoogle Scholar
  150. Weladji RB, Gaillard JM, Yoccoz NG, Holand O, Mysterud A, Loison A, Nieminen M, Stenseth NC (2006) Good reindeer mothers live longer and become better in raising offspring. Proc R Soc 273:15911239–124Google Scholar
  151. Wessells RJ, Fitzgerald E, Cypser JR, Tatar M, Bodmer R (2004) Insulin regulation of heart function in aging fruit flies. Nat Gen 21:127–1281Google Scholar
  152. Wijchers PJ, Burbach JP, Smidt MP (2006) In control of biology: of mice, men and Foxes. Biochem J 397:233–246PubMedCrossRefGoogle Scholar
  153. Wise PM, Dubal DB, Wilson ME, Rau SW, Böttner M, Rosewell KL (2001) Estradiol is a protective factor in the adult and aging brain: understanding of mechanisms derived from in vivo and in vitro studies. Brain Res Brain Res Rev 37:313–319PubMedCrossRefGoogle Scholar
  154. Witte AV, Fobker M, Gellner R, Knecht S, Floel A (2009) Caloric restriction improves memory in elderly human. Proc Natl Acad Sci 106:1255–1260PubMedCrossRefGoogle Scholar
  155. Wood JG, Rogina B, Lavu S, Howitz K, Helfand SL, Tatar M, Sinclair D (2004) Sirtuin activators mimic caloric restriction and delay aging in metazoans. Nature 430:686–689PubMedCrossRefGoogle Scholar
  156. Woolley CS, McEwen BS (1992) Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult. J Neurosci 12:2549–2554PubMedGoogle Scholar
  157. Woolley CS, McEwen BS (1993) Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J Comp Neurol 336:293–306PubMedCrossRefGoogle Scholar
  158. Woolley C.S, Gould E, Frankfurt M, McEwen B.S (1990) Long-term and short-term electrophysiological effects of estrogen on the synaptic properties of hippocampal CA1 pyramidal neurons. J Neurosci 10:4035–3225Google Scholar
  159. Xerri C, Stern JM, Merzenich MM (1994) Alterations of the cortical representation of the rat ventrum induced by nursing behavior. J Neurosci 14:1710–1721PubMedGoogle Scholar
  160. Yang Y, Hou H, Haller EM, Nicosia SV, Bai W (2005) Suppression of FOXO1 activity by FHL2 through SIRT1-mediated deacetylation. EMBO J 24:1021–1032PubMedCrossRefGoogle Scholar
  161. Yankner BA, Lu T, Loerch P (2008) The aging brain. Annu Rev Pathol 3:41–66PubMedCrossRefGoogle Scholar
  162. Yankova M, Hart SA, Woolley CS (2001) Estrogen increases synaptic connectivity between single presynaptic inputs and multiple postsynaptic CA1 pyramidal cells: a serial electron-microscopic study. Proc Natl Acad Sci 98:3525PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  • Craig Howard Kinsley
    • 2
    Email author
  • R. Adam Franssen
    • 1
  • Elizabeth Amory Meyer
    • 2
  1. 1.Department of BiologyLongwood UniversityFarmvilleUSA
  2. 2.Department of PsychologyCenter for Neuroscience, Gottwald Science Center and 116 Richmond Hall, University of RichmondRichmondUSA

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