Skip to main content
SpringerLink
Log in

The Influence of Early Life Interventions on Olfactory Memory Related to Palatable Food, and on Oxidative Stress Parameters and Na+/K+-ATPase Activity in the Hippocampus and Olfactory Bulb of Female Adult Rats

  • Original Paper
  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

The effects of neonatal handling and the absence of ovarian hormones on the olfactory memory related to a palatable food in adulthood were investigated. Oxidative stress parameters and Na+/K+-ATPase activity in the hippocampus and olfactory bulb of adult pre-puberty ovariectomized female rats handled or not in the neonatal period were also evaluated. Litters were non-handled or handled (10 min/day, days 1–10 after birth). Females from each litter were divided into: OVX (subjected to ovariectomy), sham, and intact. When adults, olfactory memory related to a palatable food (chocolate) was evaluate using the hole-board olfactory task. Additionally, oxidative stress parameters and Na+/K+-ATPase activity were measured in the hippocampus and olfactory bulb. No difference between groups was observed considering olfactory memory evaluation. Neonatal handled rats presented an increase in Na+/K+-ATPase activity in the hippocampus and in the olfactory bulb, compared to non-handled ones. Considering the surgical procedure, there was a decrease in Na+/K+-ATPase and catalase activities in sham and OVX groups, compared to intact animals in the olfactory bulb. We concluded that olfactory memory related to a palatable food in adulthood was not affected by neonatal handling or by pre-puberty surgery, with or without removal of ovaries. The difference observed between groups in catalase and Na+/K+-ATPase activity does not seem to be related to the olfactory memory. Additionally, the increase in Na+/K+-ATPase activity (an enzyme that maintains the neurochemical gradient necessary for neuronal excitability) induced by neonatal handling may be related to neuroplastic changes in the hippocampus and olfactory bulb.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Mesquita AR, Wegerich Y, Patchev AV, Oliveira M, Leão P, Sousa N, Almeida OF (2009) Glucocorticoids and neuro- and behavioural development. Semin Fetal Neonatal Med 14:130–135

    Article  PubMed  Google Scholar 

  2. Fleming AS, O’Day DH, Kraemer GW (1999) Neurobiology of mother-infant interactions: experience and central nervous system plasticity across development and generations. Neurosci Biobehav Rev 23:673–685

    Article  PubMed  CAS  Google Scholar 

  3. Mesquita AR, Pêgo JM, Summavielle T, Maciel P, Almeida OF, Sousa N (2007) Neurodevelopment milestone abnormalities in rats exposed to stress in early life. Neuroscience 147:1022–1033

    Article  PubMed  CAS  Google Scholar 

  4. Tu MT, Grunau RE, Petrie-Thomas J, Haley DW, Weinberg J, Whitfield MF (2007) Maternal stress and behavior modulate relationships between neonatal stress, attention, and basal cortisol at 8 months in preterm infants. Dev Psychobiol 49:150–164

    Article  PubMed  Google Scholar 

  5. Leon M (1992) Neuroethology of olfactory preference development. J Neurobiol 23:1557–1573

    Article  PubMed  CAS  Google Scholar 

  6. Levine S (1957) Infantile experience and resistance to physiological stress. Science 126:405–406

    Article  PubMed  CAS  Google Scholar 

  7. Meaney MJ, Diorio J, Francis D, Widdowson J, LaPlante P, Caldji C, Sharma S, Seckl JR, Plotsky PM (1996) Early environmental regulation of forebrain glucocorticoid receptor gene expression: implications for adrenocortical responses to stress. Dev Neurosci 18:49–72

    Article  PubMed  CAS  Google Scholar 

  8. Padoin MJ, Cadore LP, Gomes CM, Barros HM, Lucion AB (2001) Long-lasting effects of neonatal stimulation on the behavior of rats. Behav Neurosci 115:1332–1340

    Article  PubMed  CAS  Google Scholar 

  9. Plotsky PM, Meaney MJ (1993) Early, postnatal experience alters hypothalamic corticotrophin-releasing factor (CRF) mRNA, median eminence CRF content and stress induced release in adult rats. Brain Res Mol Brain Res 18:195–200

    Article  PubMed  CAS  Google Scholar 

  10. Silveira PP, Portella AK, Clemente Z, Bassani E, Tabajara AS, Gamaro GD, Dantas G, Torres ILS, Lucion AB, Dalmaz C (2004) Neonatal handling alters feeding behavior of adult rats. Physiol Behav 80:739–745

    Article  PubMed  CAS  Google Scholar 

  11. Raineki C, De Souza MA, Szawka RE, Lutz ML, De Vasconcellos LF, Sanvitto GL, Izquierdo I, Bevilaqua LR, Cammarota M, Lucion AB (2009) Neonatal handling and the maternal odor preference in rat pups: involvement of monoamines and cyclic AMP response element-binding protein pathway in the olfactory bulb. Neuroscience 159:31–38

    Article  PubMed  CAS  Google Scholar 

  12. Moore CL, Wong L, Daum MC, Leclair OU (1997) Mother–infant interactions in two strains of rats: implications for dissociating mechanism and function of a maternal pattern. Dev Psychobiol 30:301–312

    Article  PubMed  CAS  Google Scholar 

  13. Döhler KD, Hancke JL, Srivastava SS, Hofmann C, Shryne JE, Gorski RA (1984) Participation of estrogens in female sexual differentiation of the brain; neuroanatomical, neuroendocrine and behavioral evidence. Prog Brain Res 61:99–117

    Article  PubMed  Google Scholar 

  14. Bakker J, Honda S, Harada N, Balthazart J (2003) The aromatase knockout (ArKO) mouse provides new evidence that estrogens are required for the development of the female brain. Ann N Y Acad Sci 1007:251–262

    Article  PubMed  CAS  Google Scholar 

  15. Sanchez-Andrade G, Kendrick KM (2009) The main olfactory system and social learning in mammals. Behav Brain Res 200:323–335

    Article  PubMed  Google Scholar 

  16. Bayer SA (1983) 3H-Thymidine-radiographic studies of neurogenesis in the rat olfactory bulb. Exp Brain Res 50:329–340

    Article  PubMed  CAS  Google Scholar 

  17. Rosselli-Austin L, Altman J (1979) The postnatal development of the main olfactory bulb of the rat. J Dev Physiol 1:295–313

    PubMed  CAS  Google Scholar 

  18. Noschang CG, Krolow R, Fontella FU, Arcego DM, Diehl LA, Weis SN, Arteni NS, Dalmaz C (2010) Neonatal handling impairs spatial memory and leads to altered nitric oxide production and DNA breaks in a sex specific manner. Neurochem Res 35:1083–1091

    Article  PubMed  CAS  Google Scholar 

  19. Prediger ME, Gamaro GD, Crema LM, Fontella FU, Dalmaz C (2004) Estradiol protects against oxidative stress induced by chronic variate stress. Neurochem Res 29:1923–1930

    Article  PubMed  CAS  Google Scholar 

  20. Behl C, Moosmann B, Manthey D, Heck S (2000) The female sex hormone oestrogen as neuroprotectant: activities at various levels. Novartis Found Symp 230:221–238

    Article  PubMed  CAS  Google Scholar 

  21. Behl C, Holsboer F (1999) The female sex hormone oestrogen as a neuroprotectant. Trends Pharmacol Sci 20:441–444

    Article  PubMed  CAS  Google Scholar 

  22. Streck EL, Zugno AI, Tagliari B, Franzon R, Wannmacher CM, Wajner M, Wyse AT (2001) Inhibition of rat brain Na+, K+-ATPase activity induced by homocysteine is probably mediated by oxidative stress. Neurochem Res 26:1195–1200

    Article  PubMed  CAS  Google Scholar 

  23. Petrushanko I, Bogdanov N, Bulygina E, Grenacher B, Leinsoo T, Boldyrev A, Gassmann M, Bogdanova A (2006) Na-K-ATPase in rat cerebellar granule cells is redox sensitive. Am J Physiol Regul Integr Comp Physiol 290:R916–R925

    Article  PubMed  CAS  Google Scholar 

  24. Xie Z, Askari A (2002) Na(+)/K(+)-ATPase as a signal transducer. Eur J Biochem 269:2434–2439

    Article  PubMed  CAS  Google Scholar 

  25. Noschang C, Krolow R, Arcego DM, Toniazzo AP, Huffell AP, Dalmaz C (2012) Neonatal handling affects learning, reversal learning and antioxidant enzymes activities in a sex-specific manner in rats. Int J Dev Neurosci. doi:http://dx.doi.org/10.1016/j.ijdevneu.2012.01.010

  26. Martin C, Beshel J, Kay LM (2007) An olfacto-hippocampal network is dynamically involved in odor-discrimination learning. J Neurophysiol 98:2196–2205

    Article  PubMed  Google Scholar 

  27. Massaad CA, Washington TM, Pautler RG, Klann E (2009) Overexpression of SOD-2 reduces hippocampal superoxide and prevents memory deficits in a mouse model of Alzheimer’s disease. Proc Natl Acad Sci USA 106:13576–13581

    Article  PubMed  CAS  Google Scholar 

  28. Massaad CA, Klann E (2011) Reactive oxygen species in the regulation of synaptic plasticity and memory. Antioxid Redox Signal 14:2013–2054

    Article  PubMed  CAS  Google Scholar 

  29. Jamme I, Petit E, Divoux D, Gerbi A, Maixent JM, Nouvelot A (1995) Modulation of mouse cerebral Na+,K(+)-ATPase activity by oxygen free radicals. NeuroReport 7:333–337

    PubMed  CAS  Google Scholar 

  30. Khadrawy YA, Nour NA, Aboul Ezz HS (2011) Effect of oxidative stress induced by paradoxical sleep deprivation on the activities of Na+, K+-ATPase and acetylcholinesterase in the cortex and hippocampus of rat. Transl Res 157:100–107

    Article  PubMed  CAS  Google Scholar 

  31. Silveira PP, da Silva BenettiC, Ayres C, Pederiva FQ, Portella AK, Lucion AB, Dalmaz C (2006) Satiety assessment in neonatally handled rats. Behav Brain Res 173:205–210

    Article  PubMed  Google Scholar 

  32. da S Benetti C, Silveira PP, Portella AK, Diehl LA, Nunes E, de Oliveira VS, Dalmaz C, Goldani MZ (2007) Could preference for palatable foods in neonatally handled rats alter metabolic patterns in adult life? Pediatr Res 62:405–411

    Google Scholar 

  33. Sapolsky RM, Meaney MJ (1986) Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Res 396:64–76

    Article  PubMed  CAS  Google Scholar 

  34. Pryce CR, Ruedi-Bettschen D, Dettling AC, Feldon J (2005) Early-life environmental manipulations in rodents and primates: potential animal models in depression research. In: Steckler T, Kalin NH, Reul JMHM (eds) Handbook of stress and the brain. The Netherlands, Amsterdam, pp 23–50

    Google Scholar 

  35. Silveira PP, Portella AK, Assis SA, Nieto FB, Diehl LA, Crema LM, Peres W, Costa G, Scorza C, Quillfeldt JA, Lucion AB, Dalmaz C (2010) Early life experience alters behavioral responses to sweet food and accumbal dopamine metabolism. Int J Dev Neurosci 28:111–118

    Article  PubMed  CAS  Google Scholar 

  36. Mello e Souza T, Rohden A, Meinhardt M, Gonçalves CA, Quillfeldt JA (2000) S100B Infusion into the rat hippocampus facilitates memory for the inhibitory avoidance task but not for the open-field habituation. Physiol Behav 71:29–33

    Google Scholar 

  37. Delmas-Beauvieux MC, Peuchant E, Dumon MF, Receveur MC, Le Bras M, Clerc M (1995) Relationship between red blood cell antioxidant enzymatic system status and lipoperoxidation during the acute phase of malaria. Clin Biochem 28:163–169

    Article  PubMed  CAS  Google Scholar 

  38. Wendel A (1981) Glutathione peroxidase. Methods Enzymol 77:325–333

    Article  PubMed  CAS  Google Scholar 

  39. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  PubMed  CAS  Google Scholar 

  40. Lebel CP, Ischiropoulos H, Bondy SC (1992) Evaluation of the probe 2′,7′-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol 5:227–231

    Article  PubMed  CAS  Google Scholar 

  41. Riddles PW, Blakeley RL, Zerner B (1983) Reassessment of Ellman’s reagent. Methods Enzymol 91:49–60

    Article  PubMed  CAS  Google Scholar 

  42. de Souza Wyse AT, Streck EL, Worm P, Wajner A, Ritter F, Netto CA (2000) Preconditioning prevents the inhibition of Na+,K+-ATPase activity after brain ischemia. Neurochem Res 25:971–975

    Article  PubMed  Google Scholar 

  43. Chan KM, Delfert D, Junger KD (1986) A direct colorimetric assay for Ca2+-stimulated ATPase activity. Anal Biochem 157:375–380

    Article  PubMed  CAS  Google Scholar 

  44. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  45. Bradford MM (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  PubMed  CAS  Google Scholar 

  46. Todeschin AS, Winkelmann-Duarte EC, Jacob MH, Aranda BC, Jacobs S, Fernandes MC, Ribeiro MF, Sanvitto GL, Lucion AB (2009) Effects of neonatal handling on social memory, social interaction, and number of oxytocin and vasopressin neurons in rats. Horm Behav 56:93–100

    Article  PubMed  CAS  Google Scholar 

  47. Hlinák Z (1993) Social recognition in ovariectomized and estradiol-treated female rats. Horm Behav 27:159–166

    Article  PubMed  Google Scholar 

  48. Silveira PP, Portella AK, Benetti Cda S, Zugno AI, Scherer EB, Mattos CB, Wyse AT, Lucion AB, Dalmaz C (2011) [Association between Na+,K+-ATPase activity and the vulnerability/resilience to mood disorders induced by early life experience. Neurochem Res 36:2075–2082

    Article  PubMed  CAS  Google Scholar 

  49. da S Benetti C, Silveira PP, Matté C, Stefanello FM, Leite MC, Gonçalves CA, Wyse AT, Dalmaz C, Goldani MZ (2010) Effects of a chronic exposure to a highly palatable diet and its withdrawal, in adulthood, on cerebral Na+,K+-ATPase and plasma S100B in neonatally handled rats. Int J Dev Neurosci 28:153–159

  50. Hernández J, Condés-Lara M (1992) Brain Na+/K(+)-ATPase regulation by serotonin and norepinephrine in normal and kindled rats. Brain Res 593:239–244

    Article  PubMed  Google Scholar 

  51. Peña-Rangel MT, Mercado R, Hernández-Rodríguez J (1999) Regulation of glial Na+/K+-ATPase by serotonin: identification of participating receptors. Neurochem Res 24:643–649

    Article  PubMed  Google Scholar 

  52. Hernández-R J (1992) Na+/K(+)-ATPase regulation by neurotransmitters. Neurochem Int 20:1–10

    Article  PubMed  Google Scholar 

  53. Arborelius L, Eklund MB (2007) Both long and brief maternal separation produces persistent changes in tissue levels of brain monoamines in middle-aged female rats. Neuroscience 145:738–750

    Article  PubMed  CAS  Google Scholar 

  54. Arcego DM, Noschang C, Krolow R, Fitarelli LD, Laureano D, Huffell AP, Fontella FU, Dalmaz C (2011) Early life interventions: prepuberty stress alters oxidative parameters in distinct CNS structures in adult female rats. J Med Sci 2:741–749

    Google Scholar 

  55. Halliwell B (2001) Role of free radicals in the neurodegenerative diseases: therapeutic implications for antioxidant treatment. Drugs Aging 18:685–716

    Article  PubMed  CAS  Google Scholar 

  56. Haber F, Weiss J (1934) The catalytic decomposition of hydrogen peroxide by iron salts. Proc R Soc Lond 147:332–351

    Article  CAS  Google Scholar 

  57. Cochrane CG (1991) Mechanisms of oxidant injury of cells. Mol Aspects Med 12:137–147

    Article  PubMed  CAS  Google Scholar 

  58. Andersen SL (2003) Trajectories of brain development: point of vulnerability or window of opportunity? Neurosci Biobehav Rev 27:3–18

    Article  PubMed  Google Scholar 

  59. Buwalda B, Geerdink M, Vidal J, Koolhaas JM (2011) Social behavior and social stress in adolescence: a focus on animal models. Neurosci Biobehav Rev 35:1713–1721

    Article  PubMed  Google Scholar 

  60. Krolow R, Noschang C, Weis SN, Pettenuzzo LF, Huffell AP, Arcego DM, Marcolin M, Mota CS, Kolling J, Scherer EBS, Wyse ATS, Dalmaz C (2012) Isolation stress during the prepubertal period in rats induces long-lasting neurochemical changes in the prefrontal cortex. Neurochem Res. (In press)

Download references

Acknowledgments

This study was supported by grants from National Research Council of Brazil (CNPq) (476065/2010-0) and FAPERGS-PRONEX (10/0018.3).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Departamento de Bioquímica, ICBS, Universidade Federal do Rio Grande do Sul, Rua Ramiro Barcelos, 2600 Anexo, Porto Alegre, RS, 90035-003, Brazil

    Cristie Noschang, Rachel Krolow, Danusa M. Arcego, Daniela Laureano, Luiza D. Fitarelli, Ana Paula Huffell, Andréa G. K. Ferreira, Aline A. da Cunha, Fernanda Rossato Machado, Angela T. S. Wyse & Carla Dalmaz

Authors
  1. Cristie Noschang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rachel Krolow
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Danusa M. Arcego
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Daniela Laureano
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Luiza D. Fitarelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ana Paula Huffell
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Andréa G. K. Ferreira
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Aline A. da Cunha
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Fernanda Rossato Machado
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Angela T. S. Wyse
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Carla Dalmaz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cristie Noschang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Noschang, C., Krolow, R., Arcego, D.M. et al. The Influence of Early Life Interventions on Olfactory Memory Related to Palatable Food, and on Oxidative Stress Parameters and Na+/K+-ATPase Activity in the Hippocampus and Olfactory Bulb of Female Adult Rats. Neurochem Res 37, 1801–1810 (2012). https://doi.org/10.1007/s11064-012-0793-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-012-0793-2

Keywords

Search

Navigation