Skip to main content

Advertisement

Log in

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

  • Published:
AGE Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • 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 14:386–395

    Article  PubMed  Google Scholar 

  • 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 171:1216–1227

    Article  CAS  PubMed  Google Scholar 

  • 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 132:560–567

    Article  CAS  PubMed  Google Scholar 

  • 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 18:52–58

    Article  PubMed  Google Scholar 

  • Altarejos JY, Montminy M (2011) CREB and the CRTC co-activators: sensors for hormonal and metabolic signals. Nat Rev Mol Cell Biol 12:141–151

    Article  CAS  PubMed  Google Scholar 

  • Arner ES (2009) Focus on mammalian thioredoxin reductases—important selenoproteins with versatile functions. Biochim Biophys Acta 1790:495–526

    Article  CAS  PubMed  Google Scholar 

  • 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 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • 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 14:195–199

    Article  PubMed  Google Scholar 

  • 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 1358:172–183

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 55:208–213

    Article  CAS  PubMed  Google Scholar 

  • Chen MJ, Russo-Neustadt AA (2005) Exercise activates the phosphatidylinositol 3-kinase pathway. Brain Res Mol Brain Res 135:181–193

    Article  CAS  PubMed  Google Scholar 

  • Chen MJ, Russo-Neustadt AA (2009) Running exercise-induced up-regulation of hippocampal brain-derived neurotrophic factor is CREB-dependent. Hippocampus 19:962–972

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Colcombe S, Kramer AF (2003) Fitness effects on the cognitive function of older adults: a meta-analytic study. Psychol Sci 14:125–130

    Article  PubMed  Google Scholar 

  • Colcombe SJ, Erickson KI, Scalf PE et al (2006) Aerobic exercise training increases brain volume in aging humans. J Gerontol A: Biol Med Sci 61:1166–1170

    Article  Google Scholar 

  • Cotman CW, Berchtold NC (2002) Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci 25:295–301

    Article  CAS  PubMed  Google Scholar 

  • Cotman CW, Engesser-Cesar C (2002) Exercise enhances and protects brain function. Exerc Sport Sci Rev 30:75–79

    Article  PubMed  Google Scholar 

  • Cotman CW, Berchtold NC, Christie LA (2007) Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci 30:464–472

    Article  CAS  PubMed  Google Scholar 

  • 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 105:17–23

    Article  PubMed  Google Scholar 

  • 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 40:506–511

    Article  PubMed  Google Scholar 

  • 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 102:3811–3816

    Article  PubMed Central  PubMed  Google Scholar 

  • Erickson KI, Prakash RS, Voss MW et al (2009) Aerobic fitness is associated with hippocampal volume in elderly humans. Hippocampus 19:1030–1039

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 108:3017–3022

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 144:1193–1208

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hillman CH, Erickson KI, Kramer AF (2008) Be smart, exercise your heart: exercise effects on brain and cognition. Nat Rev Neurosci 9:58–65

    Article  CAS  PubMed  Google Scholar 

  • Kim JJ, Diamond DM (2002) The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev Neurosci 3:453–462

    CAS  PubMed  Google Scholar 

  • 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 538:54–59

    Article  CAS  PubMed  Google Scholar 

  • Kramer AF, Erickson KI (2007) Capitalizing on cortical plasticity: influence of physical activity on cognition and brain function. Trends Cogn Sci 11:342–348

    Article  PubMed  Google Scholar 

  • 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 434:245–251

    Article  CAS  PubMed  Google Scholar 

  • Larson EB (2010) Prospects for delaying the rising tide of worldwide, late-life dementias. Int Psychogeriatr 22:1196–1202

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 53:67–73

    Article  CAS  PubMed  Google Scholar 

  • 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 70:470–476

    Article  CAS  PubMed  Google Scholar 

  • 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 16:1107–1116

    Article  PubMed  Google Scholar 

  • 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 133:291–299

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nichol KE, Parachikova AI, Cotman CW (2007) Three weeks of running wheel exposure improves cognitive performance in the aged Tg2576 mouse. Behav Brain Res 184:124–132

    Article  PubMed Central  PubMed  Google Scholar 

  • Nogueira CW, Rocha JB (2011) Toxicology and pharmacology of selenium: emphasis on synthetic organoselenium compounds. Arch Toxicol 85:1313–1359

    Article  CAS  PubMed  Google Scholar 

  • 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 906:157–163

    Article  CAS  PubMed  Google Scholar 

  • Nogueira CW, Zeni G, Rocha JB (2004) Organoselenium and organotellurium compounds: toxicology and pharmacology. Chem Rev 104:6255–6285

    Article  CAS  PubMed  Google Scholar 

  • Paulmier C (1986) Selenoorganic functional groups. In: Paulmier C (ed) Selenium reagents and intermediates in organic synthesis, 1st edn. Pergamon Press, Oxford, pp 25–51

    Google Scholar 

  • 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 189:35–39

    Article  CAS  PubMed  Google Scholar 

  • 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 49:387–392

    Article  CAS  PubMed  Google Scholar 

  • 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 137:187–196

    Article  CAS  Google Scholar 

  • 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 341:217–220

    Article  CAS  PubMed  Google Scholar 

  • 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 48:9–16

    Article  CAS  PubMed  Google Scholar 

  • 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 39:127–132

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 107:219–229

    Article  CAS  PubMed  Google Scholar 

  • Silva AJ, Kogan JH, Frankland PW, Kida S (1998) CREB and memory. Annu Rev Neurosci 21:127–148

    Article  CAS  PubMed  Google Scholar 

  • Small SA, Schobel SA, Buxton RB, Witter MP, Barnes CA (2011) A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat Rev Neurosci 12:585–601

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 9:393–402

  • Souza AC, Bruning CA, Leite MR, Zeni G, Nogueira CW (2010) Diphenyl diselenide improves scopolamine-induced memory impairment in mice. Behav Pharmacol 21:556–562

    Article  CAS  PubMed  Google Scholar 

  • 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 1201:106–113

    Article  CAS  PubMed  Google Scholar 

  • Stangherlin EC, Rocha JB, Nogueira CW (2009) Diphenyl ditelluride impairs short-term memory and alters neurochemical parameters in young rats. Pharmacol Biochem Behav 91:430–435

    Article  CAS  PubMed  Google Scholar 

  • Suijo K, Inoue S, Ohya Y et al (2013) Resistance exercise enhances cognitive function in mouse. Int J Sports Med 34:368–375

    CAS  PubMed  Google Scholar 

  • Suzuki A, Fukushima H, Mukawa T et al (2011) Upregulation of CREB-mediated transcription enhances both short- and long-term memory. J Neurosci 31:8786–8802

    Article  CAS  PubMed  Google Scholar 

  • 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 121:324–334

    Article  PubMed  Google Scholar 

  • van Praag H (2009) Exercise and the brain: something to chew on. Trends Neurosci 32:283–290

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 96:13427–13431

    Article  PubMed Central  PubMed  Google Scholar 

  • van Praag H, Kempermann G, Gage FH (1999b) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2:266–270

    Article  PubMed  Google Scholar 

  • van Praag H, Shubert T, Zhao C, Gage FH (2005) Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 25:8680–8685

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 19:283–295

    Article  PubMed  Google Scholar 

  • Vaynman S, Ying Z, Gomez-Pinilla F (2004) Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci 20:2580–2590

    Article  PubMed  Google Scholar 

  • 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 144:825–833

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 21:411–422

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gilson Zeni.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cechella, J.L., Leite, M.R., Rosario, A.R. et al. Diphenyl diselenide-supplemented diet and swimming exercise enhance novel object recognition memory in old rats. AGE 36, 9666 (2014). https://doi.org/10.1007/s11357-014-9666-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11357-014-9666-8

Keywords

Navigation