AGE

, 36:9666 | Cite as

Diphenyl diselenide-supplemented diet and swimming exercise enhance novel object recognition memory in old rats

  • José L. Cechella
  • Marlon R. Leite
  • Alisson R. Rosario
  • Tuane B. Sampaio
  • Gilson Zeni
Article

Abstract

The benefits of exercise and the element selenium on mental health and cognitive performance are well documented. The purpose of the present study was to investigate whether the intake of a diet supplemented with diphenyl diselenide [(PhSe)2] and the swimming exercise could enhance memory in old Wistar rats. Male Wistar rats (24 months) were fed daily with standard diet chow or standard chow supplemented with 1 ppm of (PhSe)2 during 4 weeks. Animals were submitted to swimming training with a workload (3 % of body weight, 20 min/day for 4 weeks). After 4 weeks, the object recognition test (ORT) and the object location test (OLT) were performed. The results of this study demonstrated that intake of a supplemented diet with (PhSe)2 and swimming exercise was effective in improving short-term and long-term memory as well as spatial learning, increasing the hippocampal levels of phosphorylated cAMP-response element-binding protein (CREB) in old rats. This study also provided evidence that (PhSe)2-supplemented diet facilitated memory of old rats by modulating cAMP levels and stimulating CREB phosphorylation, without altering the levels of Akt.

Keywords

Selenium Organoselenium Exercise Memory Age 

Notes

Acknowledgments

The financial support by UFSM, CAPES, FAPERGS/CNPq (PRONEX), and research grant FAPERGS no. 10/0711-6 is gratefully acknowledged. G.Z. is a recipient of CNPq fellowship.

Conflict of interest

The authors declare no conflict of interests in the present study.

References

  1. Aarsland D, Sardahaee FS, Anderssen S, Ballard C (2010) Is physical activity a potential preventive factor for vascular dementia? A systematic review. Aging Ment Health 14:386–395PubMedCrossRefGoogle Scholar
  2. Aguiar AS Jr, Boemer G, Rial D et al (2010) High-intensity physical exercise disrupts implicit memory in mice: involvement of the striatal glutathione antioxidant system and intracellular signaling. Neuroscience 171:1216–1227PubMedCrossRefGoogle Scholar
  3. Aguiar AS Jr, Castro AA, Moreira EL et al (2011) Short bouts of mild-intensity physical exercise improve spatial learning and memory in aging rats: involvement of hippocampal plasticity via AKT, CREB and BDNF signaling. Mech Ageing Dev 132:560–567PubMedCrossRefGoogle Scholar
  4. Akbaraly TN, Hininger-Favier I, Carriere I, Arnaud J, Gourlet V, Roussel AM, Berr C (2007) Plasma selenium over time and cognitive decline in the elderly. Epidemiology 18:52–58PubMedCrossRefGoogle Scholar
  5. Altarejos JY, Montminy M (2011) CREB and the CRTC co-activators: sensors for hormonal and metabolic signals. Nat Rev Mol Cell Biol 12:141–151PubMedCrossRefGoogle Scholar
  6. Arner ES (2009) Focus on mammalian thioredoxin reductases—important selenoproteins with versatile functions. Biochim Biophys Acta 1790:495–526PubMedCrossRefGoogle Scholar
  7. Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254PubMedCrossRefGoogle Scholar
  8. Brightwell JJ, Smith CA, Neve RL, Colombo PJ (2007) Long-term memory for place learning is facilitated by expression of cAMP response element-binding protein in the dorsal hippocampus. Learn Mem 14:195–199PubMedCrossRefGoogle Scholar
  9. Chaddock L, Erickson KI, Prakash RS et al (2010) A neuroimaging investigation of the association between aerobic fitness, hippocampal volume, and memory performance in preadolescent children. Brain Res 1358:172–183PubMedCentralPubMedCrossRefGoogle Scholar
  10. Chae CH, Kim HT (2009) Forced, moderate-intensity treadmill exercise suppresses apoptosis by increasing the level of NGF and stimulating phosphatidylinositol 3-kinase signaling in the hippocampus of induced aging rats. Neurochem Int 55:208–213PubMedCrossRefGoogle Scholar
  11. Chen MJ, Russo-Neustadt AA (2005) Exercise activates the phosphatidylinositol 3-kinase pathway. Brain Res Mol Brain Res 135:181–193PubMedCrossRefGoogle Scholar
  12. Chen MJ, Russo-Neustadt AA (2009) Running exercise-induced up-regulation of hippocampal brain-derived neurotrophic factor is CREB-dependent. Hippocampus 19:962–972PubMedCentralPubMedCrossRefGoogle Scholar
  13. Colcombe S, Kramer AF (2003) Fitness effects on the cognitive function of older adults: a meta-analytic study. Psychol Sci 14:125–130PubMedCrossRefGoogle Scholar
  14. Colcombe SJ, Erickson KI, Scalf PE et al (2006) Aerobic exercise training increases brain volume in aging humans. J Gerontol A: Biol Med Sci 61:1166–1170CrossRefGoogle Scholar
  15. Cotman CW, Berchtold NC (2002) Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci 25:295–301PubMedCrossRefGoogle Scholar
  16. Cotman CW, Engesser-Cesar C (2002) Exercise enhances and protects brain function. Exerc Sport Sci Rev 30:75–79PubMedCrossRefGoogle Scholar
  17. Cotman CW, Berchtold NC, Christie LA (2007) Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci 30:464–472PubMedCrossRefGoogle Scholar
  18. de Bem AF, Portella Rde L, Colpo E et al (2009) Diphenyl diselenide decreases serum levels of total cholesterol and tissue oxidative stress in cholesterol-fed rabbits. Basic Clin Pharmacol Toxicol 105:17–23PubMedCrossRefGoogle Scholar
  19. de Lima MN, Laranja DC, Caldana F, Bromberg E, Roesler R, Schroder N (2005) Reversal of age-related deficits in object recognition memory in rats with l-deprenyl. Exp Gerontol 40:506–511PubMedCrossRefGoogle Scholar
  20. De Rosa R, Garcia AA, Braschi C, Capsoni S, Maffei L, Berardi N, Cattaneo A (2005) Intranasal administration of nerve growth factor (NGF) rescues recognition memory deficits in AD11 anti-NGF transgenic mice. Proc Natl Acad Sci U S A 102:3811–3816PubMedCentralPubMedCrossRefGoogle Scholar
  21. Erickson KI, Prakash RS, Voss MW et al (2009) Aerobic fitness is associated with hippocampal volume in elderly humans. Hippocampus 19:1030–1039PubMedCentralPubMedCrossRefGoogle Scholar
  22. Erickson KI, Voss MW, Prakash RS et al (2011) Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci U S A 108:3017–3022PubMedCentralPubMedCrossRefGoogle Scholar
  23. Greenwood BN, Strong PV, Foley TE, Thompson RS, Fleshner M (2007) Learned helplessness is independent of levels of brain-derived neurotrophic factor in the hippocampus. Neuroscience 144:1193–1208PubMedCentralPubMedCrossRefGoogle Scholar
  24. Hillman CH, Erickson KI, Kramer AF (2008) Be smart, exercise your heart: exercise effects on brain and cognition. Nat Rev Neurosci 9:58–65PubMedCrossRefGoogle Scholar
  25. Kim JJ, Diamond DM (2002) The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev Neurosci 3:453–462PubMedGoogle Scholar
  26. Kim SE, Ko IG, Shin MS, Kim CJ, Jin BK, Hong HP, Jee YS (2013) Treadmill exercise and wheel exercise enhance expressions of neutrophic factors in the hippocampus of lipopolysaccharide-injected rats. Neurosci Lett 538:54–59PubMedCrossRefGoogle Scholar
  27. Kramer AF, Erickson KI (2007) Capitalizing on cortical plasticity: influence of physical activity on cognition and brain function. Trends Cogn Sci 11:342–348PubMedCrossRefGoogle Scholar
  28. Kwon DH, Kim BS, Chang H, Kim YI, Jo SA, Leem YH (2013) Exercise ameliorates cognition impairment due to restraint stress-induced oxidative insult and reduced BDNF level. Biochem Biophys Res Commun 434:245–251PubMedCrossRefGoogle Scholar
  29. Larson EB (2010) Prospects for delaying the rising tide of worldwide, late-life dementias. Int Psychogeriatr 22:1196–1202PubMedCentralPubMedCrossRefGoogle Scholar
  30. Leite MR, Marcondes Sari MH, de Freitas ML, Oliveira LP, Dalmolin L, Brandao R, Zeni G (2014) Caffeine and diphenyl diselenide improve long-term memory impaired in middle-aged rats. Exp Gerontol 53:67–73PubMedCrossRefGoogle Scholar
  31. Maciel EN, Flores EM, Rocha JB, Folmer V (2003) Comparative deposition of diphenyl diselenide in liver, kidney, and brain of mice. Bull Environ Contam Toxicol 70:470–476PubMedCrossRefGoogle Scholar
  32. Molteni R, Ying Z, Gomez-Pinilla F (2002) Differential effects of acute and chronic exercise on plasticity-related genes in the rat hippocampus revealed by microarray. Eur J Neurosci 16:1107–1116PubMedCrossRefGoogle Scholar
  33. Morris KA, Gold PE (2012) Age-related impairments in memory and in CREB and pCREB expression in hippocampus and amygdala following inhibitory avoidance training. Mech Ageing Dev 133:291–299PubMedCentralPubMedCrossRefGoogle Scholar
  34. Nichol KE, Parachikova AI, Cotman CW (2007) Three weeks of running wheel exposure improves cognitive performance in the aged Tg2576 mouse. Behav Brain Res 184:124–132PubMedCentralPubMedCrossRefGoogle Scholar
  35. Nogueira CW, Rocha JB (2011) Toxicology and pharmacology of selenium: emphasis on synthetic organoselenium compounds. Arch Toxicol 85:1313–1359PubMedCrossRefGoogle Scholar
  36. Nogueira CW, Rotta LN, Perry ML, Souza DO, da Rocha JB (2001) Diphenyl diselenide and diphenyl ditelluride affect the rat glutamatergic system in vitro and in vivo. Brain Res 906:157–163PubMedCrossRefGoogle Scholar
  37. Nogueira CW, Zeni G, Rocha JB (2004) Organoselenium and organotellurium compounds: toxicology and pharmacology. Chem Rev 104:6255–6285PubMedCrossRefGoogle Scholar
  38. Paulmier C (1986) Selenoorganic functional groups. In: Paulmier C (ed) Selenium reagents and intermediates in organic synthesis, 1st edn. Pergamon Press, Oxford, pp 25–51Google Scholar
  39. Prigol M, Schumacher RF, WayneNogueira C, Zeni G (2009) Convulsant effect of diphenyl diselenide in rats and mice and its relationship to plasma levels. Toxicol Lett 189:35–39PubMedCrossRefGoogle Scholar
  40. Radak Z, Toldy A, Szabo Z et al (2006) The effects of training and detraining on memory, neurotrophins and oxidative stress markers in rat brain. Neurochem Int 49:387–392PubMedCrossRefGoogle Scholar
  41. Ravi Kiran T, Subramanyam MVV, Asha Devi S (2004) Swim exercise training and adaptations in the antioxidant defense system of myocardium of old rats: relationship to swim intensity and duration. Comp Biochem Physiol 137:187–196CrossRefGoogle Scholar
  42. Rosa RM, Flores DG, Appelt HR, Braga AL, Henriques JA, Roesler R (2003) Facilitation of long-term object recognition memory by pretraining administration of diphenyl diselenide in mice. Neurosci Lett 341:217–220PubMedCrossRefGoogle Scholar
  43. Schweitzer NB, Alessio HM, Berry SD, Roeske K, Hagerman AE (2006) Exercise-induced changes in cardiac gene expression and its relation to spatial maze performance. Neurochem Int 48:9–16PubMedCrossRefGoogle Scholar
  44. Serezani CH, Ballinger MN, Aronoff DM, Peters-Golden M (2008) Cyclic AMP: master regulator of innate immune cell function. Am J Respir Cell Mol Biol 39:127–132PubMedCentralPubMedCrossRefGoogle Scholar
  45. Shen H, Tong L, Balazs R, Cotman CW (2001) Physical activity elicits sustained activation of the cyclic AMP response element-binding protein and mitogen-activated protein kinase in the rat hippocampus. Neuroscience 107:219–229PubMedCrossRefGoogle Scholar
  46. Silva AJ, Kogan JH, Frankland PW, Kida S (1998) CREB and memory. Annu Rev Neurosci 21:127–148PubMedCrossRefGoogle Scholar
  47. Small SA, Schobel SA, Buxton RB, Witter MP, Barnes CA (2011) A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat Rev Neurosci 12:585–601PubMedCentralPubMedCrossRefGoogle Scholar
  48. Smorgon C, Mari E, Atti AR, Dalla Nora E, Zamboni PF, Calzoni F, Passaro A, Fellin R (2004) Trace elements and cognitive impairment: an elderly cohort study. Arch Gerontol Geriatr Suppl 9:393–402Google Scholar
  49. Souza AC, Bruning CA, Leite MR, Zeni G, Nogueira CW (2010) Diphenyl diselenide improves scopolamine-induced memory impairment in mice. Behav Pharmacol 21:556–562PubMedCrossRefGoogle Scholar
  50. Stangherlin EC, Luchese C, Pinton S, Rocha JB, Nogueira CW (2008) Sub-chronical exposure to diphenyl diselenide enhances acquisition and retention of spatial memory in rats. Brain Res 1201:106–113PubMedCrossRefGoogle Scholar
  51. Stangherlin EC, Rocha JB, Nogueira CW (2009) Diphenyl ditelluride impairs short-term memory and alters neurochemical parameters in young rats. Pharmacol Biochem Behav 91:430–435PubMedCrossRefGoogle Scholar
  52. Suijo K, Inoue S, Ohya Y et al (2013) Resistance exercise enhances cognitive function in mouse. Int J Sports Med 34:368–375PubMedGoogle Scholar
  53. Suzuki A, Fukushima H, Mukawa T et al (2011) Upregulation of CREB-mediated transcription enhances both short- and long-term memory. J Neurosci 31:8786–8802PubMedCrossRefGoogle Scholar
  54. Van der Borght K, Havekes R, Bos T, Eggen BJ, Van der Zee EA (2007) Exercise improves memory acquisition and retrieval in the Y-maze task: relationship with hippocampal neurogenesis. Behav Neurosci 121:324–334PubMedCrossRefGoogle Scholar
  55. van Praag H (2009) Exercise and the brain: something to chew on. Trends Neurosci 32:283–290PubMedCentralPubMedCrossRefGoogle Scholar
  56. van Praag H, Christie BR, Sejnowski TJ, Gage FH (1999a) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci U S A 96:13427–13431PubMedCentralPubMedCrossRefGoogle Scholar
  57. van Praag H, Kempermann G, Gage FH (1999b) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2:266–270PubMedCrossRefGoogle Scholar
  58. van Praag H, Shubert T, Zhao C, Gage FH (2005) Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 25:8680–8685PubMedCentralPubMedCrossRefGoogle Scholar
  59. Vaynman S, Gomez-Pinilla F (2005) License to run: exercise impacts functional plasticity in the intact and injured central nervous system by using neurotrophins. Neurorehabil Neural Repair 19:283–295PubMedCrossRefGoogle Scholar
  60. Vaynman S, Ying Z, Gomez-Pinilla F (2004) Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci 20:2580–2590PubMedCrossRefGoogle Scholar
  61. Vaynman S, Ying Z, Gomez-Pinilla F (2007) The select action of hippocampal calcium calmodulin protein kinase II in mediating exercise-enhanced cognitive function. Neuroscience 144:825–833PubMedCentralPubMedCrossRefGoogle Scholar
  62. Wei Z, Belal C, Tu W, Chigurupati S, Ameli NJ, Lu Y, Chan SL (2012) Chronic nicotine administration impairs activation of cyclic AMP-response element binding protein and survival of newborn cells in the dentate gyrus. Stem Cells Dev 21:411–422PubMedCrossRefGoogle Scholar

Copyright information

© American Aging Association 2014

Authors and Affiliations

  • José L. Cechella
    • 1
  • Marlon R. Leite
    • 1
  • Alisson R. Rosario
    • 1
  • Tuane B. Sampaio
    • 1
  • Gilson Zeni
    • 1
  1. 1.Laboratório de Síntese, Reatividade e Avaliação Farmacológica e Toxicológica de Organocalcogênios, Centro de Ciências Naturais e ExatasUniversidade Federal de Santa MariaSanta MariaBrazil

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