Malnutrition and brain development: An analysis of the effects of inadequate diet during different stages of life in rat

Neuroscience and Biobehavioral Reviews

Volumn 36, Issue 6, 2012, Pages 1463-1480

  Alamy, Meryem ^a   Bengelloun, Wail A ^a  

^a FACULTÉ DES SCIENCES   (Morocco)

Author keywords

Behavioral effects; Body weight; Neuroanatomical aspects; Protein malnutrition; Rat; Undernutrition

Indexed keywords

ADRENALIN; AMPHETAMINE; APOMORPHINE; ARGININE; BENZODIAZEPINE; CHLORDIAZEPOXIDE; CORTICOSTERONE; CORTICOTROPIN; DIAZEPAM; DOPAMINE RECEPTOR BLOCKING AGENT; DOPAMINE RECEPTOR STIMULATING AGENT; HALOPERIDOL; HOMOVANILLIC ACID; LYSINE; METHIONINE; NORADRENALIN; PHENYLALANINE; SEROTONIN; SUPEROXIDE DISMUTASE; TRYPTOPHAN;

ANIMAL BEHAVIOR; ANXIETY; APOPTOSIS; BEHAVIOR CHANGE; BIRTH; BODY WEIGHT; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN REGION; CELL LOSS; COGNITION; COGNITIVE DEFECT; DEVELOPMENTAL STAGE; DIET RESTRICTION; DIETARY INTAKE; DOPAMINERGIC SYSTEM; ENZYME ACTIVITY; FOOD DEPRIVATION; HABITUATION; LACTATION; LIPID PEROXIDATION; LONG TERM POTENTIATION; MATERNAL DEPRIVATION; MOTOR ACTIVITY; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEUROTRANSMITTER RELEASE; NONHUMAN; ONSET AGE; OXIDATIVE STRESS; PERINATAL PERIOD; PREGNANCY; PRENATAL PERIOD; PRIORITY JOURNAL; PROTEIN CALORIE MALNUTRITION; PROTEIN MALNUTRITION; REVIEW; SEROTONINERGIC SYSTEM; SYNAPTIC TRANSMISSION; TASK PERFORMANCE; WEANING; WEIGHT REDUCTION;

AGING; ANIMALS; BODY WEIGHT; BRAIN; DIET; PROTEIN DEFICIENCY; RATS;

EID: 84859902774     PISSN: 01497634     EISSN: 18737528     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2012.03.009     Document Type: Review

References (152)

1. Abercrombie E.D., Keefe K.A., Difrischia D.S., Zigmond M.J. Differential effect of stress on in vivo dopamine release in striatum, nucleus accumbens and medial frontal cortex. Journal of Neurochemistry 1989, 52:1655-1658.
2. Agale S., Kulkarni A., Ranjekar P., Joshi S. Maternal caloric restriction spares fetal brain polyunsaturated fatty acids in wistar rats. Brain and Development 2010, 32:123-129.
3. Agarwal D.K., Awasthy A., Upadhyay S.K., Singh P., Kumar J., Agarwal K.N. Growth, behavior, development and intelligence in rural children between 1-3 years of life. Indian Pediatrics 1992, 29:467-480.
4. Agharanya J.C., Wurtman R.J. Effect of dietary proteins and carbohydrates on urinary and sympathoadrenal catecholamines. Neurochemistry International 1985, 7(2):271-277.
5. Alamy M., Errami M., Taghzouti K., Sadiki-Traki F., Bengelloun W.A. Effects of postweaning undernutrition on behavior, memory and sensory reactivity in rats: implications of the dopaminergic system. Physiology & Behavior 2005, 86:195-202.
6. Alfaro-Rodrigez A., Gonzales-Pina R., Gonzales-Marciel A., Arch-Tirado E. Serotonin and 5-hydroxy-indole-acetic acid contents in dorsal raphe and suprachiasmatic nuclei in normal, malnourished and rehabilitated rats under 24h of sleep deprivation. Brain Research 2006, 1110:95-101.
7. Almeida S.S., De Araujo M. Postnatal protein malnutrition affects play behaviour and other social interactions in juvenile rats. Physiology & Behavior 2001, 74:45-51.
8. Almeida S.S., Tonkiss J., Galler J.R. Malnutrition and reactivity to drugs acting in the central nervous system. Neuroscience & Biobehavioral Reviews 1996, 20:389-402.
9. Almeida S.S., Tonkiss J., Galler J.R. Prenatal protein malnutrition affects avoidance but not escape behavior in the elevated T-maze. Physiology & Behavior 1996, 60(1):191-195.
10. Almeida S.S., Tonkiss J., Galler J.R. Prenatal Protein malnutrition affects the social interactions of juvenile rats. Physiology & Behavior 1996, 60(1):197-201.
11. Almeida S.S., Soares E.G., Bichuette M.Z., Graeff F.G., De Oliveira L.M. Effects of early postnatal malnutrition and chlordiazepoxide on experimental aversive situations. Physiology & Behavior 1992, 51(6):1195-1199.
12. Andrade J.P., Cadete-Leite A., Madeira M.D., Paula-Barbosa M.M. Long-term low-protein diet reduces the number of hippocampal mossy fiber synapses. Experimental Neurology 1991, 112(1):119-124.
13. Bedi K.S. Effects of undernutrition in early life on granule cell numbers in the rat dentate gyrus. The Journal of Comparative Neurology 1991, 311:425-433.
14. Bedi K.S. Lasting neuroanatomical changes following undernutrition during early life. Early Nutrition and Later Achievement 1987, 2-49. Academic Press, London. J. Dobbing (Ed.).
15. Bengelloun W.A. Kwashiorkor: behavioural indices of neurological sequelae. (Mal) Nutrition and the Infant Brain 1990, Wiley-Liss, Inc., pp. 65-81.
16. Berkman D.S., Lescano A.G., Gilman R.H., Lopez S.L., Black M.M. Effects of stunting, diarrhoeal disease, and parasitic infection during infancy on cognition in late childhood: a follow-up study. Lancet 2002, 359:564-571.
17. Bertrand J., Klos A., Debski B. Content of polyunsaturated fatty acids (PUFAs) in serum and liver of rats fed restricted diets supplemented with vitamins B2, B6 and acid folic acid. Biofactors 2004, 22:189-192.
18. Blatt G.J., Chen J., Rosene D.L., Volicer L., Galler J.R. Prenatal protein malnutrition effects on the serotoninergic system in the hippocampal formation: an immunocytochemical, ligand binding, and neurochemical study. Brain Research Bulletin 1994, 34:507-518.
19. Bonatto F., Polydoro M., Andrades M.E., Conte da Frota M.L., Dal-Pizzol F., Rotta L.N., Souza D.O., Perry M.L., Moreira J.C.F. Effect of protein malnutrition on redox state of the hippocampus of rat. Brain Research 2005, 1:17-22.
20. Borghese C.M., Córdoba N.E., Laino C.H., Orsingher O.A., Rubio C.M., Niselman V. Lack of tolerance to the anxiolytic effect of diazepam and pentobarbital following chronic administration in perinatally undernourished rats. Brain Research Bulletin 1998, 46(3):237-244.
21. Brioni J.D., Orsingher O.A. Operant behavior and reactivity to the anticonflict effect of diazepam in perinatally undernourished rats. Physiology & Behavior 1998, 44:193-198.
22. Brioni J.D., Cordoba N., Orsingher O.A. Decreased reactivity to the anticonflict effect of diazepam in perinatally undernourished rats. Behavioural Brain Research 1989, 34:159-162.
23. Brioni J.D., Keller E.A., Levin L.E., Cordoba N.E., Orsingher O.A. Reactivity to amphetamine in perinatally undernourished rats: behavioral and neurochemical correlates. Pharmacology, Biochemistry, and Behavior 1986, 24:449-454.
24. Bronzino J.D., Blaise J.H., Mokler D.J., Galler J.R., Morgane P.J. Modulation of paired-pulse responses in the dentate gyrus: effects of prenatal protein malnutrition. Brain Research 1999, 849:45-57.
25. Bronzino J.D., Austin-La France P.J., Mokler D.J., Morgane P.J. Effects of prenatal protein malnutrition on hippocampal long-term potentiation in freely moving rats. Experimental Neurology 1997, 148:317-323.
26. Bronzino J.D., Blaise J.H., Austin-LaFrance P.J., Morgane P.J. Studies of dentate granule cell modulation: paired-pulse responses in freely moving rats at three ages. Developmental Brain Research 1996, 96:277-280.
27. Bronzino J.D., Abu-Hassaballah P.J., Austin-LaFrance R.J., Morgane P.J. Maturation of long term potentiation in the hippocampal dentate gyrus of the freely moving rat. Hippocampus 1994, 4:439-446.
28. Bronzino J.D., Austin-LaFrance R.J., Morgane P.J., Galler J.R. Effects of prenatal protein malnutrition on kindling induced alterations in dentate granule cell excitability: paired pulse measures. Experimental Neurology 1991, 112:216-223.
29. Camargo L.M.M., Almeida S.S. Early postnatal protein malnutrition changes the development of social play in rats. Physiology & Behavior 2005, 85(3):246-251.
30. Castro C.A., Rudy J.W. Early-life malnutrition selectively retards the development of distal- but not proximal-cue navigation. Developmental Psychobiology 1987, 20:251-537.
31. Chen J.C., Turiak G., Galler J.R., Volicer L. Postnatal changes of brain monoamine levels in prenatally malnourished and control rats. International Journal of Developmental Neuroscience 1997, 15(2):257-263.
32. Chen J.C., Tonkiss J., Galler J.R., Volicer L. Prenatal protein malnutrition in rats enhances serotonin release from hippocampus. The Journal of Nutrition 1992, 122:2138-2143.
33. Chiel H.J., Wurtman R.J. Short-term variations in diet composition change the pattern of spontaneous motor activity in rats. Science 1981, 213:676-678.
34. Cintra L., Aguilar A., Granados L., Galvan A., Kemper T., Debassio W.A. Effects of prenatal protein malnutrition on mossy fibers of the hippocampal formation in rats of three age groups. Hippocampus 1997, 7:184-191.
35. Cintra L., Diaz-Cintra S., Galvan A., Kemper T., Morgane P.J. Effects of protein undernutrition on the dentate Gyrus in rats of three age groups. Brain Research 1990, 532:271-277.
36. Curtis H.C., Niederwieser A., Visconti M. Serotonin and dopamine synthesis in phenylketonuria. Serotonin: Current Aspects of Neurochemistry and Function 1982, 277-289. Plenum Publ. Corp., New York. B. Haber (Ed.).
37. Davis E., Zhang K., Tarazi F.I., Baldessarini R.J. Animal models of attention-deficit hyperactivity disorder. Brain Research Reviews 2003, 42:1-21.
38. Debassio W.A., Kemper T.L., Tonkiss J., Galler J.R. Effect of prenatal protein deprivation on postnatal granule cell generation in the hippocampal dentate gyrus. Brain Research Bulletin 1996, 41(6):379-383.
39. Debassio W.A., Kemper T.L., Galler J.R., Tonkiss J. Prenatal malnutrition effect on pyramidal and granule cell generation in the hippocampal formation. Brain Research Bulletin 1994, 35(1):57-61.
40. Del Arco A., Segovia G., De Blas M., Garrido P., Acuña-Castroviejo D., Pamplona R., Mora F. Prefrontal cortex, caloric restriction and stress during aging: studies on dopamine and acetylcholine release, BDNF and working memory. Behavioural Brain Research 2011, 216(1):136-145.
41. De Rooij S.R., Wouters H., Yonker J.E., Painter R.C., Roseboom T.J. Prenatal undernutrition and cognitive function in late adulthood. Proceedings of the National Academy of Sciences 2010, 107(39):16881-16886.
42. D'Hooge R., De Deyn P.P. Applications of the Morris water maze in the study of learning and memory. Brain Research Reviews 2001, 36:60-90.
43. Dhopeshwarkar G.A. Nutrition and Brain Development 1983, Plenum Press, New York.
44. Díaz-Cintra S., González-Maciel A., Morales M.A., Aguilar A., Cintra L., Prado-Alcalá R.A. Protein malnutrition differentially alters the number of glutamic acid decarboxylase-67 interneurons in dentate gyrus and CA1-3 subfields of the dorsal hippocampus. Experimental Neurology 2007, 208(1):47-53.
45. Díaz-Cintra S., García-Ruiz M., Corkidi G., Cintra L. Effects of prenatal malnutrition and postnatal nutritional rehabilitation on CA3 hippocampal pyramidal cells in rats of four ages. Brain Research 1994, 662:117-126.
46. Díaz-Cintra S., Diaz-Cintra L., Galvan A., Aguilar A., Kemper T.L., Morgane P.J. Effects of prenatal protein deprivation on postnatal development of granule cells in the fascia dentate. The Journal of Comparative Neurology 1991, 310:356-364.
47. Dietrich M.O., Mantese C.E., Anjos G.M., Rotta L.N., Perry M.L.S., Souza D.O., Lara D.R. Increased locomotor response to amphetamine, but not other psychostimulants, in adult mice submitted to a low-protein diet. Physiology & Behavior 2004, 83:129-133.
48. Dobbing J. Early Nutrition and Later Achievement 1987, Academic Press, London.
49. Dobbing J. Effects of experimental undernutrition on development of the nervous system. Malnutrition, Learning and Behaviour 1968, 181-202. M.I.T. Press, Boston. N.S. Scrimshaw, J.E. Gordon (Eds.).
50. Feoli A.M., Leite M.C., Tramontina A.C., Tramontina F., Posser T., Rodrigues L., Swarowsky A., Quincozes-Santos A., Leal R.B., Gottfried C., Perry M.L.S., Gonçalves C.A. Developmental changes in content of glial marker proteins in rats exposed to protein malnutrition. Brain Research 2008, 1187(2):33-41.
51. Feoli A.M., Ionara R., Almeida L.S., Tramontina A.C., Vanzella C., Sbaraini S., Schweigert I.D., Netto C.A., Perry M.L.S., Gonçalves C.A. Effects of protein malnutrition on oxidative status in rat brain. Nutrition 2006, 22(2):160-165.
52. Fernandez S.F., Menendez M.F., Fernandez B.M., Patterson A.M. Malnutrition in utero and during lactation in the rat: relationship of dams weight gain and development of suckling. Nutrition Research 1985, 5(4):413-421.
53. Fukuda M.T.H., Silva A.L.F., Almeida S.S. Early postnatal protein malnutrition affects learning and memory in the distal but not in the proximal cue version of the Morris water maze. Behavioural Brain Research 2002, 133:271-277.
54. Françolin-Silva A.L., Hernandes A.S., Fukuda M.T.H., Valadares C.T., Almeida S.S. Anxiolytic-like effects of short-term postnatal protein malnutrition in the elevated plus maze test. Behavioural Brain Research 2006, 173:310-314.
55. Galler R.J., Shumsky J.S., Morgane P.J. Malnutrition and brain development. Nutrition in Pediatrics. Part II 1997, 196-212. Hamilton, London. W.A. Walker, B.C. Decker (Eds.).
56. Galler J.R., Tonkiss J. Prenatal protein malnutrition and maternal behavior in Sprague-Dawley rats. The Journal of Nutrition 1991, 121:762-769.
57. Galler J.R., Ramsey F.C., Morley D.S., Archer E., Salt P. The long-term effects of early kwashiorkor compared with marasmus. IV. Performance on the national high school entrance examination. Pediatric Research 1990, 28:235-239.
58. Galler J.R., Ramsey F.C., Forde V., Salt P., Archer E. Long-term effects of early kwashiorkor compared with marasmus. II. Intellectual performance. Journal of Pediatric Gastroenterology and Nutrition 1987, 6:847-854.
59. Galler J.R., Propert K.J. Maternal behavior following rehabilitation of rats with intergenerational malnutrition. 1. Persistent changes in lactation-related behaviors. The Journal of Nutrition 1981, 111:1330-1336.
60. Garcia Y.J., Rodriguez-Malaver L.A.J., Penaloza N. Lipid peroxidation measurement by thiobarbituric acid assay in rat cerebellar slices. Journal of Neuroscience Methods 2005, 15(144):127-135.
61. García-Ruiz M., Díaz-Cintra S., Cintra L., Corkidi G. Effect of protein malnutrition on CA3 hippocampal pyramidal cells in rats of three ages. Brain Research 1993, 22:203-212.
62. Goodlett C.R., Nonneman A.J., Valentino M.L., West J.R. Constraints on water maze spatial learning in rats: implications for behavioral studies of brain damage and recovery of function. Behavioural Brain Research 1988, 28(3):275-286.
63. Granados-Rojas L., Larriva-Sahd L., Cintra L., Gutiérrez-Ospina G., Rondán A., Díaz-Cintra S. Prenatal protein malnutrition decreases mossy fibers-CA3 thorny excrescences asymmetrical synapses in adult rats. Brain Research 2002, 933(2):164-171.
64. Gressens P., Muaku S.M., Besse L., Nsegbe L., Gallego J., Delpech B., Gaultier C., Evrard P., Ketelslegers J.M., Maiter D. Maternal protein restriction early in rat pregnancy alters brain development in the progeny. Developmental Brain Research 1997, 103(1):21-35.
65. Halliwell B., Gutterdridge J.M.C. Free Radicals in Biology and Medecine 2006, Clarendon Press, Oxford. 4th ed.
66. Hawkins R.A., Robyn R.L., Simpson I.A., Vina J.R. Structure of the blood-brain barrier and its role in the transport of amino acids. The Journal of Nutrition 2006, 136:218S-226S.
67. Hernandes A.S., Françolin-Silva A.L., Valadares C.T., Fukuda M.T.H., Almeida S.S. Effects of different malnutrition techniques on the behavior of rats tested in the elevated T-maze. Behavioural Brain Research 2005, 162(2):240-245.
68. Hernandez J.R., Manjarrez G.G., Chagoya G. Newborn humans and rats malnourished in utero: free plasma L-tryptophan, neutral amino acids and brain serotonin synthesis. Brain Research 1989, 488:1-13.
69. Serine-133 phosphorylation. Developmental Brain Research 2003, 145(2):213-218.
70. Ikeda M., Levitt M., Udenfriend S. Phenylalanine as substrate and inhibitor of tyrosine hydroxylase. Archives of Biochemistry and Biophysics 1967, 120:420-427.
71. Jahnke S., Bedi K.S. Undernutrition during early life increases the level of apoptosis in the dentate gyrus but not in the CA2+CA3 region of the hippocampal formation. Brain Research 2007, 1143:60-69.
72. Jordan T.C., Clark G.A. Early undernutrition impairs hippocampal long-term potentiation in adult rats. Behavioral Neuroscience 1983, 97(2):319-322.
73. Jordan T.C., Cane S.E., Howells K.F. Deficits in spatial memory performance induced by early undernutrition. Developmental Psychobiology 1981, 14:317-325.
74. Joshi S., Garole V., Daware M., Girigosavi S., Rao S. Maternal protein restriction before pregnancy affects vital organs of offspring in Wistar rats. Metabolism 2003, 52:13-18.
75. Kar B.R., Rao S.L., Chandramouli B.A. Cognitive development in children with chronic protein energy malnutrition. Behavioral and Brain Function 2008, 4. 31, 1-12.
76. Katz H.B., Davis C.A., Dobbing J. Effects of undernutrition at different ages early in life and later environmental complexity on parameters of the cerebellum and hippocampus in rats. The Journal of Nutrition 1982, 112:1362-1368.
77. Kehoe P., Mallinson K., Bronzino J., McCormick C.M. Effects of prenatal protein malnutrition and neonatal stress on CNS responsiveness. Developmental Brain Research 2001, 132:23-31.
78. King R.S., DeBassio W.A., Kemper T.L., Rosene D.L., Tonkiss J., Galler J.R., Blatt G.J. Effects of prenatal protein malnutrition and acute postnatal stress on granule cell genesis in the fascia dentata of neonatal and juvenile rats. Developmental Brain Research 2004, 150(1):9-15.
79. King R.S., Kemper T.L., Debassio W.A., Ramzan M., Blatt G.J., Rosene D.L., Galler J.R. Birthdates and number of neurons in the serotoninergic raphe nuclei in the rat with prenatal protein malnutrition. Nutritional Neuroscience 2002, 5:391-397.
80. Kosten T.A., Zhang X.Y., Kehoe P. Infant rats with chronic neonatal isolation experiencehow decreased extracellular serotonin levels in ventral striatum at baseline and in response to cocaine. Developmental Brain Research 2004, 152:19-24.
81. Laus M.F., Vales L.D.M.F., Costa T.M.B., Almeida S.S. Early postnatal protein-calorie malnutrition and cognition: a review of human and animal studies. International Journal of Environmental Research and Public Health 2011, 8:590-612.
82. Leahy J.P., Stern W.C., Resnick O., Morgane P.J. A neuropharmacological analysis of central nervous system catecholamine systems in developmental protein malnutrition. Developmental Psychobiology 1978, 11(4):361-370.
83. Levay E.A., Paolini A.G., Govic A., Hazia A., Penmana J., Kent S. HPA and sympathoadrenal activity of adult rats perinatally exposed to maternal mild caloric restriction. Behavioural Brain Research 2010, 208:202-208.
84. Levay E.A., Paolini A.G., Govic A., Hazia A., Penmana A., Kent S. Anxiety-like behaviour in adult rats perinatally exposed to maternal calorie restriction. Behavioural Brain Research 2008, 191:164-172.
85. Levay E.A., Govic A., Penman J., Paolini A.G., Kent S. Effects of adult-onset calorie restriction on anxiety-like behavior in rats. Physiology & Behavior 2007, 92:889-896.
86. Lieberman H.R., Yeghiayan S.K., Maher T.J. A low protein diet alters behavior and neurotransmission in normothermic and hyperthermic environments. Brain Research Bulletin 2005, 66:149-154.
87. Lieberman H.R., Askew E.W., Hoyt R.W., Shukitt-Hale B., Sharp M.A. Effects of thirty days of undernutrition on plasma neurotransmitter precursors, other amino acids and behavior. The Journal of Nutritional Biochemistry 1997, 8:119-126.
88. Lou H.C., Lykkelund C., Gerdes A.M., Udesen H., Bruhn P. Increased vigilance and dopamine synthesis by large doses of tyrosine or phenylalanine restriction in phenylketonuria. Acta Paediatrica Scandinavica 1987, 76:560-565.
89. Lukoyanov N.V., Andrade J.P. Behavioral effects of protein deprivation and rehabilitation in adult rats: relevance to morphological alterations in the hippocampal formation. Behavioural Brain Research 2000, 112:85-97.
90. Masur J., Ribiero M.J. Chronic starvation impairs the effect of depressant drugs on CNS of rats. Pharmacology 1981, 23:64-68.
91. Mathangi D.C., Namasivayam A. Effect of chronic protein restriction on motor co-ordination and brain neurotransmitters in albino rats. Food and Chemical Toxicology 2001, 39:1039-1043.
92. Matos R.J.B., Orozco-Solís R., Lopes de Souza S., Manhães-de-Castro R., Bolaños-Jiménez F. Nutrient restriction during early life reduces cell proliferation in the hippocampus at adulthood but does not impair the neuronal differentiation process of the new generated cells. Neuroscience 2011, 196:16-24.
93. Mazer C., Muneyyirci J., Taheny K., Raio N., Borella A., Whitaker-Azmitia P. Serotonin depletion during synaptogenesis leads to decreased synaptic density and learning deficits in the adult rat: a possible model of neurodevelopmental disorders with cognitive deficits. Brain Research 1997, 760:68-73.
94. Mendez M.A., Adair L.S. Severity and timing of stunting in the first two years of life affect performance on cognitive tests in late childhood. The Journal of Nutrition 1999, 129:1555-1562.
95. Menon N.K., Dhopeshwarkar G.A. Essential fatty acid deficiency and lipid metabolism of the developing brain. Progress in Lipid Research 1981, 20:129-134.
96. Miller M., Hasson R., Resnick O. Availability of phenylalanine and tyrosine for brain norepinephrine synthesis in developmentally protein malnourished rats. Experimental Neurology 1982, 77:163-178.
97. Miranda M.C., Nóbrega F.J., Sato K., Pompéia S., Sinnes E.G., Bueno O.F.A. Neuropsychology and malnutrition: a study with 7 to 10 years-old children in a poor community. Revista Brasileira de Saúde Materno Infantil. 2007, 7:45-54.
98. Mohapel J.G., Boehme F., Kainer L., Christie B.R. Hippocampal cell loss and neurogenesis after fetal alcohol exposure: insights from different rodent models. Brain Research Reviews 2010, 64(2):283-303.
99. Mokler D.J., Torres O.I., Galler J.R., Morgane P.J. Stress-induced changes in extracellular dopamine and serotonin in the medial prefrontal cortex and dorsal hippocampus of prenatally malnourished rats. Brain Research 2007, 1148:226-233.
100. Mokler D.J., Galler J.R., Morgane P.J. Modulation of 5-HT release in the hippocampus of 30-day-old rats exposed in utero to protein malnutrition. Developmental Brain Research 2003, 142(2):203-208.
101. Mokler D.J., Bronzino J.D., Galler J.R., Morgane P.J. Effects of median raphé electrical stimulation on serotonin release in the dorsal hippocampal formation of prenatally malnourished rats. Brain Research 1999, 838(12):95-103.
102. Morgane P.J., Mokler D.J., Galler J.R. Effects of prenatal protein malnutrition on the hippocampal formation. Neuroscience & Biobehavioral Reviews 2002, 26(4):471-484.
103. Morgane P.J., Austin-LaFrance R.J., Bronzino J.D., Tonkiss J., Diaz-Cintra S., Cintra L., Kemper T., Galler J.R. Malnutrition and the developing central nervous system. The Vulnerable Brain: Nutrition and Toxins 1992, 3-44. Plenum Press, New York. R.L. Issacson, K.F. Jensen (Eds.).
104. Morgane P.J., Miller M., Kemper T., Stern W.C., Forbes W., Hall R., Bronzino J.D., Caisson J., Hawrylewicz E., Resnick O. The effects of protein malnutrition on the developing central nervous system of the rat. Neuroscience & Biobehavioral Reviews 1978, 2:137-230.
105. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. Journal of Neuroscience Methods 1984, 11:47-60.
106. Olivier P., Olivier B., Bouslama M.P., Gressens P., Verney C. Moderate growth restriction: deleterious and protective effects on white matter damage. Neurobiology of Disease 2007, 26:253-263.
107. Palmer A.A., Brownc A.S., Keegand D., DeSanti Siskad L., Sussere E., Rotrosend J., Butler P.D. Prenatal protein deprivation alters dopamine-mediated behaviors and dopaminergic and glutamatergic receptor binding. Brain Research 2008, 1237:62-74.
108. Palmer A.A., Printz D.J., Butler P.D., Dulawa S.C., Printz M.P. Prenatal protein deprivation in rats induces changes in prepulse inhibition and NMDA receptor binding. Brain Research 2004, 996(2):193-201.
109. Paula-Barbosa M.M., Andrade J.P., Castedo J.L. Cell loss in the cerebellum and hippocampal formation of adult rats after long-term low protein diet. Experimental Neurology 1989, 103:186-193.
110. Partadiredja G., Worrall S., Simpson R., Bedi K.S. Pre-weaning undernutrition alters the expression levels of reactive oxygen species enzymes but not their activity levels or lipid peroxidation in the rat brain. Brain Research 2008, 1222:69-78.
111. Pereira-da-Silva M.S., Cabral-Filho J.E., De Olivera M.L. Effect of early malnutrition and environmental stimulation in the performance of rats in the elevated plus maze. Behavioural Brain Research 2009, 205:286-289.
112. Prakash S. Malnutrition and undernutrition. Medicine 2006, 31:18-22.
113. Ranade S.C., Rose A., Rao M., Gallego J., Gressens P., Mani S. Different types of nutritional deficiencies affect different domains of spatial memory function checked in a radial arm maze. Neuroscience 2008, 152:859-866.
114. Resnick O., Morgane P.J. Ontogeny of the levels of serotonin in various parts of the brain in severely protein malnourished rats. Brain Research 1984, 303(1):163-170.
115. Reyes-Castro L.A., Rodriguez J.S., Rodríguez-González G.L., Wimmer R.D., McDonald T.J., Larrea F., Nathanielsz P.W., Zambrano E. Pre- and/or postnatal protein restriction in rats impairs learning and motivation in male offspring. International Journal of Developmental Neuroscience 2011, 29:177-182.
116. Rocinholi L.F., Landeira-Fernandez J. Anxiety-like behavior in weanling and young adult rat male and female malnourished rats. Physiology & Behavior 2011, 102:13-16.
117. Rosenberg M. Global child health: burden of disease, achievements and future challenges. Current Problems in Pediatric and Adolescent Health Care 2007, 37:338-362.
118. Rotta L.N., Schmidt A.P., Souza T.M., Nogueira C.W., Souza K.B., Izquerdo I., Perry M.L., Souza D.O. Effects of undernutrition on glutamatergic parameters in rat brain. Neurochemical Research 2003, 28:1181-1186.
119. Santucci L.B., Daud M.M., Almeida S.S., De Oliveira L.M. Effects of early protein malnutrition and environmental stimulation upon the reactivity to diazepam in two animal models of anxiety. Pharmacology, Biochemistry, and Behavior 1994, 49(2):393-398.
120. Schweiger U., Warnhoff M., Pirke K.M. Brain tyrosine availability and the depression of central nervous norepinephrine turnover in acute and chronic starvation in adult male rats. Brain Research 1985, 335(2):207-212.
121. Scrimshaw N.S., Gordon J.E. Malnutrition Learning and Behavior; Proceedings 1968, M.I.T. Press, Cambridge.
122. Shoemaker O., Wurtman O. Perinatal undernutrition: accumulation of cathecolamine in rat brain. Science 1971, 171:1017-1019.
123. Shultz P.L., Tonkiss J., Morgane P.J., Bronzino J.D., Galler J.R. Effects of an every other day rapid kindling procedure in prenatally protein malnourished rats. Brain Research 1995, 682:35-40.
124. Smart J.L., Whatson T.S., Dobbing J. Thresholds of response to electric shock in previously undernourished rats. The Journal of Nutrition 1975, 34:511-516.
125. Souza A.S., Fernandes F.S., Tavares do Carmo M.G. Effects of maternal malnutrition and postnatal nutritional rehabilitation on brain fatty acids, learning, and memory. Nutrition Reviews 2011, 69(3):132-144.
126. Souza A.S., Pacheco L.C., Castro P.S., Hokoç J.N., Rocha M.S., Tavares do Carmo M.G. Brain fatty acid profiles and spatial learning in malnourished rats: effects of nutritional intervention. Nutritional Neuroscience 2008, 11:119-127.
127. Soto-Moyano R., Fernandez V., Sanhueza M., Belmar J., Kusch C., Perez H., Ruiz S., Hernandez A. Effects of mild protein prenatal malnutrition and subsequent postnatal nutritional rehabilitation on noradrenaline release and neuronal density in the rat occipital cortex. Developmental Brain Research 1999, 116(1):51-58.
128. Steiger J.L., Alexander M.J., Galler J.R., Farb D.H., Russek S.J. Effects of prenatal malnutrition on GABAA receptor alpha1, alpha3 and beta2 mRNA levels. Neuroreport 2003, 15:1731-1735.
129. Steiger J.L., Galler J.R., Farb D.H., Russek S.J. Prenatal protein malnutrition reduces beta2, beta 3 and gamma 2L GABA (A) receptor subunit mRNAs in the adult septum. European Journal of Pharmacology 2002, 446:201-202.
130. Stone E.A. Stress and cathecolamines. Cathecolamines and Behaviour, Vol. 2, Neuropsychopharmacology 1975, 31-72. Plenum Press, New York. A.J. Friedhoff (Ed.).
131. Tatli M., Guzel A., Kiizil G., Kavak V., Yavuz M., Kizil M. Comparison of the effects of maternal protein malnutrition and intrauterine growth restriction on redox state of central nervous system in offspring rats. Brain Research 2007, 1156:21-30.
132. Tonkiss J., Galler J.R. Prenatal malnutrition alters diazepam-mediated suppression of ultrasonic vocalizations in an age dependent manner. Behavioural Brain Research 2007, 182(2):337-343.
133. Tonkiss J., Trzcinska M., Shultz P., Vincitore M., Galler J.R. Prenatally protein malnourished rats are less sensitive to the amnestic effects of medial septal infusions of chlordiazepoxide. Behavioural Pharmacology 2000, 11:437-446.
134. Tonkiss J., Shultz P.L., Shumsky J.S., Fiacco T.A., Vincitore M., Rosene D.L., Galler J.R. Chlordiazepoxide-induced learning deficits: dose-dependent differences following prenatal malnutrition. Pharmacology, Biochemistry, and Behavior 2000, 65:105-116.
135. Tonkiss J., Shultz P., Galler J.R. An analysis of spatial navigation in prenatally protein malnourished rats. Physiology & Behavior 1994, 55:217-224.
136. Tonkiss J., Galler J.R., Morgane P.J., Bronzino J., Austin-LaFrance R.J. Prenatal protein malnutrition and postnatal brain function. Annals of the New York Academy of Sciences 1993, 678:215-227.
137. Tonkiss J., Galler J.R., Shukitt-Hale B., Rocco F.J. Prenatal protein malnutrition impairs visual discrimination learning in adult rats. Psychobiology 1991, 19:247-250.
138. Tonkiss J., Galler J.R., Formica R.N., Rocco F.J., Galler J.R. Fetal protein malnutrition impairs acquisition of DRL task in adults rats. Physiology & Behavior 1990, 48:73-77.
139. Tonkiss J., Shukitt-Hale B., Formica R.N., Rocco F.J., Galler J.R. Prenatal protein malnutrition alters response to reward in adult rats. Physiology & Behavior 1990, 48(5):675-680.
140. Trzcinska M., Tonkiss J., Galler J.R. Influence of prenatal protein malnutrition on behavioural reactivity to stress in adult rats. Stress 1999, 3(1):71-83.
141. Valdomero A., Bussolino D.F., Orsingher O.A., Cuadra G.R. Perinatal protein malnutrition enhances rewarding cocaine properties in adult rats. Neuroscience 2006, 137(1):221-229.
142. Verhagen L.A.W., Luijendi M., Korte-Bouws G.A.H., Korte S.M., Adan R.A.H. Dopamine and serotonin release in the nucleus accubens during starvation-induced hyperactivity. European Neuropsychopharmacology 2009, 19:309-316.
143. Walton E., Allen S. Malnutrition in developing countries. Paediatrics and Child health 2011, 21(9):418-424.
144. Winnick M. Malnutrition and brain development. The Journal of Pediatrics 1969, 74(5):667-679.
145. Winnick M. Changes in nucleic acid and protein content of human brain during growth. Pediatric Research 1968, 2:325-355.
146. Winnick M., Rosso P. Head circumference and cellular growth of the brain in normal and marasmic children. The Journal of Pediatrics 1969, 74:774-778.
147. Wiggins R.C., Fuller G., Enna S.J. Undernutrition and the development of brain neurotransmitter systems. Life Science 1984, 35:2085-2094.
148. Yamazaki A., Ohtsuki Y., Yoshihara T., Honma S., Honma K.I. Maternal deprivation in neonatal rats of different conditions affects growth rate, circadian clock, and stress responsiveness differentially. Physiology & Behavior 2005, 86:136-144.
149. Zamenhof S. Depletion of individuals with " Outstandingly high" cerebral development in rats subjected to prenatal undernutrition. Nutritional Research 1991, 11(6):687-690.
150. Zhang L., Corona-Morales A.A., Vega-Gonzalez A., Garcia-Estrada J., Escobar A. Dietary tryptophan restriction in rats triggers astrocyte cytoskeletal hypertrophy in hippocampus and amygdale. Neuroscience Letters 2009, 450:242-245.
151. Zhang Y., Li N., Yan Z. Perinatal food restriction impaired spatial learning and memory behaviour and decreased the density of nitric oxide synthase in neurons in the hippocampus of adult male rat offspring. Toxicology Letters 2010, 193:167-172.
152. Zhang Y., Li N., Yang J., Zhang T., Yang Z. Effects of maternal food restriction on physical growth and neurobehaviour in newborn Wistar rats. Brain Research Bulletin 2010, 83:1-8.