Effects of early protein malnutrition and environmental stimulation on behavioral and biochemical parameters in rats submitted to the elevated plus-maze test

Nutritional Neuroscience

Volumn 16, Issue 3, 2013, Pages 104-112

  Soares, Roberto O ^a   Oliveira, Luiz M ^a   Marchini, Julio S ^a   Rodrigues, José Antunes ^a   Elias, Lucila L K ^a   Almeida, Sebastião S ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Corticosterone; Elevated plus maze; Environmental enrichment; Polyamines; Protein malnutrition; Tactile stimulation

Indexed keywords

CORTICOSTERONE; POLYAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; BEHAVIOR; BODY WEIGHT; CONTROLLED STUDY; ENVIRONMENTAL ENRICHMENT; ENVIRONMENTAL FACTOR; EXPLORATORY BEHAVIOR; KWASHIORKOR; MALE; MAZE TEST; NEUROCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; RAT; RISK ASSESSMENT; TACTILE STIMULATION;

ANIMALS; BEHAVIOR, ANIMAL; BODY WEIGHT; CORTICOSTERONE; DIET; ENVIRONMENT; EXPLORATORY BEHAVIOR; HIPPOCAMPUS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; MAZE LEARNING; PITUITARY-ADRENAL SYSTEM; POLYAMINES; PROTEIN-ENERGY MALNUTRITION; RATS; RATS, WISTAR;

ANIMALIA; RATTUS;

EID: 84876085194     PISSN: 1028415X     EISSN: 14768305     Source Type: Journal    
DOI: 10.1179/1476830512Y.0000000036     Document Type: Article

References (57)

1. Levitsky DA, Barnes RH. Nutritional and environmental interactions in the behavioral development of the rat: long-term effects. Science 1972;176(4030):68-71.
2. Morgane PJ, Mokler DJ, Galler JR. Effects of prenatal protein malnutrition on the hippocampal formation. Neurosci Biobehav Rev 2002;26:471-83.
3. Kehoe P, Mallinson K, Bronzino J, McCormick CM. Effects of prenatal protein malnutrition and neonatal stress on CNS responsiveness. Brain Res Dev Brain Res 2001;132:23-31.
4. Cintra L, Granados L, Aguilar A, Kemper T, Bassio W, Galler J, et al. Effects of prenatal protein malnutrition on mossy fibers of the hippocampal formation in rats of four age groups. Hippocampus 1997;7:184-91.
5. Duran P, Galler JR, Cintra L, Tonkiss J. Prenatal malnutrition and sleep states in adult rats: effects of restraint stress. Physiol Behav 2006;89:156-63.
6. Adlard BPF, Smart JL. Adrenocortical function in rats subjected to nutritional deprivation in early life. J Endocrinol 1972;54: 99-105.
7. Sampaio VF, De Oliveira LM, Almeida SS, Marchini JS, Antunes-Rodrigues J, Elias LLK. The effects of early protein malnutrition and environmental stimulation on behavioral and biochemical parameters in rats psychol. Neuroscience 2008;1: 109-19.
8. Mesquita RM, Pereira PA, Andrade JP. Low levels of brain derived neurotrophic factor and tyrosine kinase receptor B are related to loss of dentate granule cells after prolonged lowprotein feeding in the rat. Neurosci Lett 2002;330:155-8.
9. Lister JP, Blatt GJ, Debassio WA, Kemper TL, Tonkiss J, Galler JR, et al. Effect of prenatal protein malnutrition on numbers of neurons in the principal cell layers of the adult rat hippocampal formation. Hippocampus 2005;15:393-403.
10. Gilad GM, Gilad VH. Brain polyamine stress response: recurrence after repetitive stressor and inhibition by lithium. J Neurochem 1996;67:1992-6.
11. Gilad GM, Gilad VH, Eliyayev Y, Rabey JM. Developmental regulation of the brain polyamine-stress-response. Int J DevNeurosci 1998;16:271-8.
12. Gilad VH, Rabey JM, Kimiagar Y, Gilad GM. The polyamine stress response: tissue, endocrine, and developmental-dependent regulation. Biochem Pharmacol 2001;61:207-13.
13. Seiler N. Catabolism of polyamines. Amino Acids 2004;26: 217-33.
14. Almeida SS, Garcia RM, De Oliveira LM. Effects of early protein malnutrition and repeated testing upon locomotor and exploratory behaviors in the elevated plus-maze. Physiol Behav 1993;54:749-52.
15. Francolin-Silva AL, Hernandes AS, Fukuda MTH, Valadares CT, Almeida SS. Anxiolytic-like effects of short-term postnatal protein malnutrition in the elevated plus-maze test. Behav Brain Res 2006;173:310-4.
16. Almeida SS, Soares EG, Bichuette MZ, Graeff FG, De Oliveira LM. Effects of early postnatal malnutrition and chlordiazepoxide on experimental aversive situations. Physiol Behav 1992;51: 1195-9.
17. Gomes CM, Frantz PJ, Sanvitto GL, Anselmo-Franci JA, Lucion AB. Neonatal handling induces an ovulatory estrous cycles in rats. Braz J Med Biol Res 1999;32:1239-42.
18. Lima JG, De Oliveira LM, Almeida SS. Effects of early concurrent protein malnutrition and environmental stimulation on the central nervous system and behavior. Nutr Neurosci 1999;1: 439-48.
19. Riul TR, Carvalho AF, Almeida PS, De Oliveira LM, Almeida SS. Ethological analysis of mother-pup interactions and other behavioral reactions in rats: effects malnutrition and tactile stimulation of the pups. Braz J Med Biol Res 1999;32:975-83.
20. Pryce CR, Feldon J. Long-term neurobehavioural impact of the postnatal environmental in rats: manipulations, effects and mediating mechanisms. Neurosci Biobehav Rev 2003;27:57-71.
21. Smythe JW, Rowe WB, Meaney MJ. Neonatal handling alters serotonin (5-HT) turnover and 5-HT2 receptor binding in selected brain regions: relationship to the handling effect on glucocorticoid receptor expression. Dev Brain Res 1994;80:183-9.
22. Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, Feedman A, et al. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 1997;277(5332):1659-62.
23. Wigger A, Neumann ID. Periodic maternal deprivation induces gender-dependent alterations in behavioral and neuroendocrine responses to emotional stress in adult rats. Physiol Behav 1999; 66:293-302.
24. Cancedda L, Putignano E, Sale A, Viegi A, Berardi N, Maffei L. Acceleration of visual system development by environmental enrichment. J Neurosci 2004;24:4840-8.
25. Wood DA, Buse JE, Wellman CL, Rebect GV. Differential environmental exposure alters NMDA but not AMPA receptor subunit expression in nucleus accumbens core and shell. Brain Res 2005;1042:176-83.
26. Diamond MC, Krech D, Rosenzweig MR. The effects of an enriched environment on the histology of the rat cerebral cortex. J Comp Neurol 1964;123:111-9.
27. Rosenzweig MR, Love W, Bennett EL. Effects of a few hour a day of enriched experience on brain chemistry and brain weights. Psychol Behav 1968;3:819-25.
28. Rosenzweig MR, Bennett EL. Psychobiology of plasticity: effects of training and experience on brain and behavior. Behav Brain Res 1996;78:57-65.
29. Fernandez-Teruel A, Escorihuela RM, Jimenez P, Torbena A. Infantile stimulation and perinatal administration of Ro 15-1788: additive anxiety-reducing effects in rats. Eur J Pharmacol 1990;191:111-4.
30. Santucci LB, Daud MM, Almeida SS, De Oliveira LM. Effects of early protein malnutrition and environmental stimulation upon the reactivity to diazepam in two animal models of anxiety. Pharmacol Biochem Behav 1994;49:393-8.
31. Mcintosh J, Anisman H, Merali Z. Short and long-periods of neonatal maternal separation differentially affect anxiety and feeding in adult rats: gender-dependent effects. Brain Res Dev Brain Res 1999;113:97-106.
32. Cambraia RPB, Vannucchi H, De Oliveira LM. Food intake and weight of lactating rats maintained on different protein-calorie diets, and pup growth. Braz J Med Biol Res 1997;30:985-8.
33. Pereira LO, Arteni NS, Petersen RC, Da Rocha AM, Achaval M, Netto CA. Effects of daily environmental enrichment on memory deficits and brain injury following neonatal hypoxiaischemia in the rat. Neurobiol Learn Mem 2006;87:101-8.
34. Diamond MC. Response of the brain to enrichment. An Acad Bras Ciênc 2001;73:211-20.
35. Cruz AP, Frei F, Graeff FG. Ethopharmacological analysis of rat behavior on the elevated plus-maze. Pharmacol Biochem Behav 1994;49:171-76.
36. Elias LL, Antunes-Rodrigues J, Elias PC, Moreira AC. Effect of plasma osmolality on pituitary-adrenal responses to corticotropin-releasing hormone and atrial natriuretic peptide changes in central diabetes insipidus. J Clin Endocrinol Metab 1997;82: 1243-7.
37. Elias PC, Elias LL, Castro M, Antunes-Rodrigues J, Moreira AC. Hypothalamic-pituitary-adrenal axis up-regulation in rats submitted to pituitary stalk compression. J Endocrinol 2004; 180:297-302.
38. Löser C, Wunderlich U, Fölsh UR. Reversed-phase liquid chromatographic separation and simultaneous fluorimetric detection of polyamines and theirs monoacetyl derivatives in human and animal urine, serum and tissue samples: an improved, rapid and sensitive method for routine application. J Chromatogr 1988;430:249-62.
39. Hernandes A, Almeida SS. Postnatal protein malnutrition affects inhibitory avoidance and risk assessment behaviors in two model of anxiety in rats. Nutr Neurosci 2003;6:213-9.
40. Cabral A, Almeida SS. Effects of tactile stimulation and underwater trauma on the behavior of protein-malnourished rats in the elevated plus-maze test. Psychol Neurosci 2008;1:67-72.
41. Rocinholi LF, Almeida SS, De Oliveira LM. Response threshold to aversive stimuli in stimulated early protein-malnourished rats. Braz J Med Biol Res 1997;30:407-13.
42. Fukuda MT, Françolin-Silva AL, Hernandes AS, Valadares CT, Almeida SS. Effects of early protein malnutrition and scopolamine on learning and memory in the Morris water maze. Nutr Neurosci 2007;10:251-9.
43. Almeida SS, De Oliveira LM, Graeff FG. Early life protein malnutrition changes exploration of the elevated plus-maze end reactivity to anxiolytics. Psychopharmacology 1991;103:513-8.
44. McNaughton N, Gray JA. Anxiolytic action on the behavioural inhibition system implies multiple types of arousal contribute to anxiety. J Affect Disord 2000;61:161-76.
45. File SE, Zangrossi H, Viana M, Graeff FG. Trial 2 in the elevated plus-maze: a different form of fear? Psychopharmacology 1993;111:491-4.
46. Will B, Galani R, Kelche CE, Rosenzweig MR. Recovery from brain injury in animals: relative efficacy of environmental enrichment, physical exercise or formal training (1990-2002). Prog Neurobiol 2004;72:167-82.
47. Renner MJ, Rosenweing MR. Social interactions among rats housed in grouped and enriched conditions. Dev Psychobiol 1986;19:303-13.
48. Bertoglio LJ, Carobrez AP. Previous maze experience required to increase open arms avoidance in rats submitted to the elevated plus-maze model of anxiety. Behav Brain Res 2000;108:197-203.
49. Carobrez AP, Bertoglio LJ. Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20 years on. Neurosci Biobehav Rev 2005;29:1193-205.
50. Dal-Cól MLC, Orlandi Pereira L, Rosa VP, Calixto AV, Carobrez AP, Faria MS. Lack of midazolam-induced anxiolysis in the plus-maze Trial 2 is dependent on the length of Trial 1. Pharmacol Biochem Behav 2003;74:395-400.
51. Rhee HJ, Kim EJ, Lee JK. Physiological polyamines: simple primordial stress molecules. J Cell Mol Med 2007;11:685-703.
52. Artola A, Von Frijtag JC, Fermont PCJ, Gispen WH, Schrama LH, Kamal A, et al. Long-lasting modulation of the induction of LTD and LTP in rat hippocampal CA1 by behavioural stress and environmental enrichment. Eur J Neurosci 2006;23:261-72.
53. Peña Y, Prunell M, Dimitsantos V, Nadal R, Escorihuela RM. Environmental enrichment effects in social investigation in rats are gender dependent. Behav Brain Res 2006;174:181-7.
54. Peña Y, Prunell M, Rotllant D, Armario A, Escorihuela RM. Enduring effects of environmental enrichment from weaning to adulthood on pituitary-adrenal function, pre-pulse inhibition and learning in male and female rats. Psychoneuroendocrinology 2009;34:1390-404.
55. Francolin-Silva AL, Almeida SS. The interaction of housing condition and acute immobilization stress on the elevated plusmaze behaviors of protein-malnourished rats. Braz J Med Biol Res 2004;37:1035-42.
56. Jutapakdeegul N, Casalotti SO, Govitrapong P, Kotchabahkdi N. Postnatal touch stimulation acutely alters corticosterone levels and glucocorticoid receptor gene expression in the neonatal rat. Dev Neurosci 2003;25:26-33.
57. Schanberg SM, Ingledue VF, Lee JY, Hannun YA, Bartolome JV. PKCα mediates maternal touch regulation of growth-related gene expression in infant rats. Neuropsychopharmacology 2003;28:1026-30.