Effects of postnatal protein malnutrition on learning and memory procedures

Nutritional Neuroscience

Volumn 13, Issue 6, 2010, Pages 274-282

  Valadares, C T ^a   Fukuda, M T H ^a   Francolin Silva A L ^a   Hernandes, A S ^a   Almeida, S S ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

learning; protein malnutrition; recognition memory; working memory

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; COGNITIVE DEFECT; CONTROLLED STUDY; FEMALE; LATENT PERIOD; LEARNING; MAZE TEST; MEMORY; MEMORY DISORDER; MENTAL PERFORMANCE; NONHUMAN; OPEN FIELD TEST; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN MALNUTRITION; RAT; WORD RECOGNITION; WORKING MEMORY;

ANIMALS; BODY WEIGHT; ESCAPE REACTION; LATENCY PERIOD (PSYCHOLOGY); LEARNING DISORDERS; MALE; MAZE LEARNING; MEMORY DISORDERS; PROTEIN DEFICIENCY; RATS; RATS, WISTAR; RECOGNITION (PSYCHOLOGY);

ANIMALIA; RATTUS;

EID: 78049495604     PISSN: 1028415X     EISSN: 14768305     Source Type: Journal    
DOI: 10.1179/147683010X12611460764769     Document Type: Article

References (59)

1. Andrade JP, Paula-Barbosa MM. Protein malnutrition alters the cholinergic and GABAergic system of the hippocampal formation of the adult rats: an immunocytochemical study. Neurosci Lett 1996;211:211-215.
2. Andrade JP, Madeira MD, Paula-Barbosa MM. Effects of long-term malnutrition and rehabilitation on the hippocampal formation of the adult rats: a morphometric study. J Anat 1995;187:379-393.
3. Andrade JP, Madeira MD, Paula-Barbosa MM. Evidence of reorganization in the hippocampal mossy fiber synapse of adults rats rehabilitated after prolonged undernutrition. Exp Brain Res 1995;104:249-261.
4. Andrade JP, Castanheira-Vale AJ, Paz-Dias PG et al. The dendritic trees of the neurons from the hippocampal formation of adult proteindeprived rats. A quantitative Golgi study. Exp Brain Res 1996;109:419-433.
5. Austin-Lafrance RJ, Morgane PJ, Bronzing JD. Prenatal protein malnutrition and hippocampal function: rapid kindling. Brain Res Bull 1991;27:815-818.
6. Diaz-Cintra S, Cintra L, Galvan A et al. Effects of prenatal protein deprivation on the postnatal development of granule cells in the fascia dentata. J Comp Neurol 1991;310:356-364.
7. Fukuda MTH, Françolin-Silva AL, Almeida SS. Early postnatal protein malnutrition affects learning and memory in the distal but not in the proximal cue version of the Morris water maze. Behav Brain Res 2002;133:271-277.
8. Fukuda MTH, Françolin-Silva AL, Hernandes AS et al. Effects of early protein malnutrition and scopolamine on learning and memory in the Morris water maze. Nutr Neurosci 2007;10:251-259.
9. Hernandes AS, Françolin-Silva AL, Valadares CT et al. Effects of different malnutrition techniques the behavior of rats tested in the elevated T-maze. Behav Brain Res 2005;162:240-245.
10. Lukoyanov NV, Andrade J P. Behavioral effects of protein deprivation and rehabilitation in adults rats: relevance to morphological alterations in the hippocampal formation. Behav Brain Res 2000;112:85-97.
11. Valadares CT, Almeida SS. Early protein malnutrition changes learning and memory in spaced but not in condensed trials in the Morris water maze. Nutr Neurosci 2005;8:39-47.
12. Galler JR, Shumsky JS, Morgane PJ. Malnutrition and brain development. In: Walker WA, Watkins J. (eds) Nutrition in Pediatrics. Neuilly Sur-Seine: Plenum, 1996;194-210.
13. Strupp BJ, Levitiski DA. Enduring cognitive effects of early malnutrition: a theoretical reappraisal. J Nutr 1995;125:2221-2229.
14. Hall RD. Is hippocampal function in the adult rat impaired by early protein or protein-calorie deficiencies? Dev Psychobiol 1983;16:395-411.
15. Jordan TC, Cane SE, Howells KF. Deficits in spatial memory performance induced by early undernutrition. Dev Psychobiol 1981;14:317-325.
16. Jaiswal AK, Upadhyay SN, Satyan KS et al. Comparative effects of prenatal and postnatal undernutrition on learning and memory in rats. Indian J Exp Biol 1999;37:17-22.
17. Tonkiss J, Galler JR. Prenatal protein malnutrition and working memory performance in adults rats. Behav Brain Res 1990;40:95-107.
18. Castro CA, Tracy M, Rudy J W. Early life undernutrition impairs the development of the learning and short-term memory processes mediating performance in a conditional-spatial discrimination task. Behav Brain Res 1989;32:255-264.
19. Wolf C, Almli CR, Finger S et al. Behavioral effects of severe and moderate malnutrition. Physiol Behav 1986;38:725-730.
20. Campbell LF, Bedi KS. The effects of undernutrition during early life on spatial learning. Physiol Behav 1989;45:883-890.
21. Castro AC, Rudy J W. Early-life malnutrition selectively retards the development of distal-but not proximal-cue navigation. Dev Psychobiol 1987;20:521-537.
22. Cordoba NE, Arolfo MP, Brioni JD et al. Perinatal undernutrition impairs spatial learning in recovered adult rats. Acta Physiol Pharmacol Ther Latinoam 1994;44:70-76.
23. Tonkiss J, Shultz P, Galler JR. An analysis of spatial navigation in prenatally protein malnourished rats. Physiol Behav 1994;55:217-224.
24. Tonkiss J, Galler JR, Formica RN et al. Fetal protein malnutrition impairs acquisition of a DRL task in adult rats. Physiol Behav 1990;48:73-77.
25. Bedi KS. Spatial learning ability of rats undernourished during early postnatal life. Physiol Behav 1992;51:1001-1007.
26. Bonatto F, Polydoro M, Andrades ME et al. Effect of protein malnutrition on redox state of the hippocampus of rat. Brain Res 2005;1042:17-22.
27. Diaz-Cintra S, Gonzalez-Maciel A, Morales MA et al. Protein malnutrition differentially alters the number of glutamic acid decarboxylase-67 interneurons in dentate gyrus and CA1-3 subfields of the dorsal hippocampus. Exp Neurol 2007;208:47-53.
28. Granados-Rojas L, Aguilar A, Diaz-Cintra S. The mossy fiber system of the hippocampal formation is decreased by chronic and postnatal but not by prenatal protein malnutrition in rats. Nutr Neurosci 2004;7:301-308.
29. Lister JP, Blatt GJ, DeBassio WA 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.
30. Leung LS, Shen B. Hippocampal CA1 kindling but not long-term potentiation disrupts spatial memory performance. Learn Mem 2006;13:18-26.
31. Morris RGM, Garrud P, Rawlins JNP et al. Place navigation impaired in rats with hippocampal lesions. Nature 1982;297:681-683.
32. Olton DS, Walker JA, Gage FH. Hippocampal connections and spatial discrimination. Brain Res 1978;139:295-308.
33. Save E, Poucet B. Involvement of the hippocampus and associative parietal cortex in the use of proximal and distal landmarks for navigation. Behav Brain Res 2000;109:195-206.
34. O'Keefe JB, Nadel R. The hippocampus as a cognitive map. Oxford: Clarendon, 1978.
35. Olton DS. Memory functions and the hippocampus. In: Seifert W. (ed) Neurobiology of the Hippocampus. New York: Academic Press, 1983;335-374.
36. O'Keefe J. Spatial memory within and without the hippocampal system. In: Seifert W. (ed) Neurobiology of the Hippocampus. New York: Academic Press, 1983;375-403.
37. Morris RGM. Spatial localization does not require the presence of local cues. Learn Motiv 1981;12:239-260.
38. Bedi KS. Effects of undernutrition during early life on granule cell numbers in the rat dentate gyrus. J Comp Neurol 1991;311:425-433.
39. Smart JL, Dobbing J. Increased thirst and hunger in adults rats undernourished as infants: an alternative explanation. Br J Nutr 1977;37:421-430.
40. Dodart JC, Mathis C, Ungerer, A. Scopolamine-induced deficits in a twotrial object recognition task in mice. Neuroreport 1997;8:1173-1178.
41. Manns JR, Hopkins RO, Reed JM et al. Recognition memory and the human hippocampus. Neuron 2003;37:171-180.
42. Garcia-Moreno, LM, Conejo NM, Capilla A et al. Chronic ethanol intake and object recognition in young and adult rats. Prog Neuropsychopharmacol Biol Psychiatry 2002;26:831-837.
43. Dix SL, Aggleton J P. Extending the spontaneous preference test of recognition: evidence of object - location and object - context recognition. Behav Brain Res 1999;99:191-200.
44. Ennaceur A, Aggleton JP. Spontaneous recognition of object configurations in rats: effects of fornix lesions. Exp Brain Res 1994;100:85-92.
45. Ennaceur A, Neave N, Aggleton J P. Neurotoxic lesions of the perirhinal cortex do not mimic the behavioral effects of fornix transaction in the rat. Behav Brain Res 1996;80:9-25.
46. Ennaceur A, Neave N, Aggleton J P. Spontaneous object recognition and object location memory in rats: the effect of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix. Exp Brain Res 1997;113:509-519.
47. Françolin-Silva AL, Almeida SS. The interaction of housing condition and acute immobilization stress on the elevated plus-maze behaviors of protein-malnourished rats. Braz J Med Biol Res 2004;37:1035-1042.
48. Barnes RH, Neely CS, Kwong E et al. Postnatal nutritional deprivations as determinants of adult rat behavior toward food, its consumption and utilization. J Nutr 1968;96:467-476.
49. Dobbing J. Early nutrition and later achievement. London: Academic Press, 1987.
50. Morgane PJ, Miller M, Kemper T et al. The effects of protein malnutrition on the developing central nervous system of the rat. Neurosci Biobehav Rev 1978;2:137-230.
51. Cambraia RP, 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;30:985-988.
52. Lima JG, Oliveira LM, Lachat JJ et al. Comparison of the effects of lab chow and casein diets based on body and brain development of rats. Braz J Med Biol Res 1993;26:1069-1076.
53. Passos MCF, Ramos CF, Moura EG. Short and long term effects of malnutrition in rats during lactation on the body weight of offspring. Nutr Res 2000;11:1603-1612.
54. Pothuizen HHJ, Zhang W-N, Jongen-Rêlo AL et al. Dissociation of function between the dorsal and the ventral hippocampus in spatial learning abilities of the rat: a within-subject, within-task comparison of reference and working spatial memory. Eur J Neurosci 2004;19:705-712.
55. Zhang W-N, Pothuizen HHJ, Feldon J et al. Dissociation of function within the hippocampus: effects of dorsal, ventral and complete excitotoxic hippocampal lesions on spatial navigation. Neuroscience 2004;127:289-300.
56. De Oliveira LM, Almeida SS. Effects of malnutrition and environment on the acquisition and the extinction of avoidance behavior in rats. Physiol Behav 1985;34:141-154.
57. Blokland A, Geraerts E, Been M. A detailed analysis of rats' spatial memory in a probe trial of a Morris tasks. Behav Brain Res 2004;154:71-75.
58. Clark RE, Zola SM, Squire LR. Impaired recognition memory in rats after damage to the hippocampus. J Neurosci 2000;20:8853-8860.
59. Obinu MC, Reibaud M, Miquet JM et al. Brain-selective stimulation of nicotinic receptors by TC-1734 enhances Ach transmission from frontoparietal cortex and memory in rodents. Prog Neuropsychopharmacol Biol Psychiatry 2002;26:913-918.