Differential vulnerability of the rat retina, suprachiasmatic nucleus and intergeniculate leaflet to malnutrition induced during brain development

Brain Research Bulletin

Volumn 64, Issue 5, 2005, Pages 395-408

  Vilela, M C R ^a   Mendonca J E F ^a   Bittencourt, H ^a   Lapa, R M ^a   Alessio, M L M ^a   Costa, M S M O ^c   Guedes, R C A ^b   Silva, V L ^a   Andrade Da Costa, B L S ^a  

^a LTF UFPB   (Brazil)

^b CCEN   (Brazil)

^c FEDERAL UNIVERSITY OF RIO GRANDE   (Brazil)

Author keywords

Circadian timing system; Geniculohypothalamic tract; Neuropeptide Y; Nutrition; Retinal ganglion cells; Retinohypothalamic tract

Indexed keywords

NEUROPEPTIDE Y;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL COUNT; CELL STRUCTURE; CELLULAR DISTRIBUTION; CIRCADIAN RHYTHM; CONTROLLED STUDY; DENSITOMETRY; FEMALE; GENICULATE BODY; HYPOTHALAMUS; IMMUNOREACTIVITY; MALE; MALNUTRITION; NERVE PROJECTION; NISSL STAINING; NONHUMAN; PRIORITY JOURNAL; RAT; RETINA; RETINA GANGLION CELL; SUPRACHIASMATIC NUCLEUS; THALAMUS;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BODY WEIGHT; BRAIN; CELL COUNT; CELL SIZE; FEMALE; GENICULATE BODIES; IMMUNOHISTOCHEMISTRY; LACTATION; MALE; MALNUTRITION; NEURAL PATHWAYS; NEURONS; NEUROPEPTIDE Y; ORGAN SIZE; RATS; RATS, WISTAR; RETINA; SEX FACTORS; STAINING AND LABELING; SUPRACHIASMATIC NUCLEUS;

EID: 10644250814     PISSN: 03619230     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2004.09.011     Document Type: Article

References (77)

1. K.N. Agarwal, C. Prassad, and V. Taneja Protein deprivation and the brain: effect on enzymes and free amino acids related to glutamate metabolism in rats Ann. Nutr. Metabol. 25 1981 228 233
2. R. Aguilar-Roblero, A. Salazar-Juarez, J. Rojas-Castañeda, C. Escobar, and L. Cintra Organization of circadian rhythmicity and suprachiasmatic nuclei in malnourished rats AJP- Integ. Comp. Physiol. 273 1997 1321 1331
3. M.F.L. Almeida, E.N. Yamasaki, A.C.D. Silveira, R.C.A. Guedes, and J.N. Hokoç The GABAergic and cholinergic systems in the retina are differentially affected by postnatal malnutrition during the suckling period Nutr. Neurosci. 4 2001 223 238
4. S.S. Almeida, L.H. Duntas, L. Dye, M.L. Nunes, C. Prasad, J.B.T. Rocha, P. Wainwright, C.T.B.V. Zaia, and R.C.A. Guedes Nutrition and brain function: a multidisciplinary virtual symposium Nutr. Neurosci. 5 2002 311 320
5. C.P. Almli, M.A. Henault, A. Velozco, and P.J. Morgane Ontogeny of electrical of main olfactory bulb in freely-moving normal and malnourished rats Brain Res. 350 1985 1 11
6. J. Altman, and S.A. Bayer Development of the diencephalons in the rat. IV. Quantitative study of the time of origin of neurons and the internuclear chronological gradients in the thalamus J. Comp. Neurol. 188 1979 455 471
7. A.F.D. Andrade, R.C.A. Guedes, and N.R. Teodósio Enhanced rate of cortical spreading depression due to malnutrition: prevention by dietary protein supplementation Braz. J. Med. Biol. Res. 23 1990 889 893
8. J.P. Andrade, M.D. Madeira, and M.M. Paula-Barbosa Effects of long-term malnutrition and rehabilitation on the hippocampal formation of the adult rat. A morphometric study J. Anat. 187 1995 379 393
9. A. Ballabriga Some aspects of clinical and biochemical changes related to nutrition during brain development in humans Dev. Neurobiol. 12 1989 271 285
10. J.M. Barreto Medeiros, J.E. Cabral Filho, S.L.D. Souza, S.R. Freitas Silva, C. Mendes da Silva, T.C.B.J. Deiró, J.M. Monteiro, R.C.A. Guedes, C.M.M.B. Castro, and R. Manhães de Castro Early malnourished rats are not affected by anorexia induced by a selective serotonin reuptake inhibitor in adult life Nutr. Neurosci. 5 2002 211 214
11. N.H. Bass, M.G. Netsky, and E. Young Effects of neonatal malnutrition on developing cerebrum I: microchemical and histological study of cellular differentiation in the rat Arch. Neurol. 23 1970 289 302
12. B. Beck, M. Jhanwar-Uniyal, A. Burlet, M. Chapleur-Chateau, S.F. Leibowitz, and C. Burlet Rapid and localized alterations of neuropeptide Y in discrete hypothalamic nuclei with feeding status Brain Res. 528 1990 245 249
13. J.M.C. Borba, M.S. Araújo, C.W. Picanço-Diniz, R. Manhães De Castro, and R.C.A. Guedes Permanent and transitory morphometric changes of NADPH-diaphorase-containing neurons in the rat visual cortex after early malnutrition Brain Res. Bull. 53 2000 193 201
14. L.S. Brady, M.A. Smith, P.W. Gold, and M. Herkenham Altered expression of hypothalamic neuropeptide Y mRNAs in food restricted and food deprived rats Neuroendocrinology 52 1990 441 447
15. S.M. Bunt, R.D. Lund, and P.W. Land Prenatal development of the optic projection in albino and hooded rats Dev. Brain Res. 6 1983 149 168
16. O. Castañón-Cervantes, and L. Cintra Circadian rhythms of occipital-cortex temperature and motor activity in young and old rats under chronic protein malnutrition Nutr. Neurosci. 5 2002 279 286
17. J.-C. Chen, J. Tonkiss, J.R. Galler, and L. Volicer Prenatal protein malnutrition in rats enhances serotonin release from hippocampus J. Nutr. 122 1992 2138 2143
18. L. Cintra, S. Diaz-Cintra, A. Galván, and P.J. Morgane Circadian rhythm of sleep in normal and undernourished rats Bol. Estud. Méd. Biol. Méx. 36 1988 3 17
19. L. Cintra, P. Durán, M.A. Guevara, A. Aguilar, and O. Castañón-Cervantes Pre- and post-natal protein malnutrition alters the effect of rapid eye movements sleep-deprivation by the platform-technique upon the electrocorticogram of the circadian sleep-wake cycle and its frequency bands in the rat Nutr. Neurosci. 5 2002 91 101
20. L. Cintra, A. Galván, S. Diaz-Cintra, and C. Escobar Protein malnutrition on suprachiasmatic nucleus cells in rats of three ages Bol. Estud. Méd. Biol. Méx. 42 1994 11 19
21. J. Cipolla Neto, E.G.I.G. Recine, L. Menna-Barreto, N. Marques, S.C. Afeche, C. Schott, G. Fortunato, R.B. Sothern, and F. Halberg Perinatal Malnutrition, Suprachiasmatic Nuclear Lesioning, and Circadian-Ultradian Aspects of Spontaneous Behavior of Albino Rats Advances in Chronobiology Part B 1987 Wiley-Liss New York pp. 473-489
22. F.B. Costa, J.A. Costa, J.E. Cabral Filho, R.C.A. Guedes, N.R. Teodósio, Indicadores de maduracion nerviosa y somática en un modelo experimental de desnutricion, in: Seminário Internacional "Desnutricion y Funciones Cerebrales Superiores", Resumenes de Conferências e Comunicaciones Libres, Santiago, Universidad de las Naciones Unidas, 1983, p. 89.
23. S.P.M. Costa, Influência de uma desnutrição multifatorial na composição dos ácidos graxos de fosfolipídeos do sistema nervoso central e fígado em diferentes períodos do desenvolvimento do rato. Recife, Master Thesis - Universidade Federal de Pernambuco, 2003.
24. E.M. Coutinho, L.P.C.G. Freitas, and F.G.G. Abath The influence of the regional basic diet from northeast Brazil on health and nutritional conditions of mice infected with Schistosoma mansoni Rev. Soc. Bras. Med. Trop. 25 1992 13 20
25. S. Datta, E.H. Patterson, M. Vincitore, J. Tonkiss, P.J. Morgane, and J.R. Galler Prenatal protein malnourished rats show changes in sleep-wake behavior as adults J. Sleep Res. 9 2000 71 79
26. M. Desai, and C.N. Hales Role of fetal and infant growth in programming metabolism in later life Biol. Rev. 72 1997 329 348
27. S. Diaz-Cintra, L. Cintra, A. Galván, A. Aguilar, T. Kemper, and P.J. Morgane Effects of prenatal protein deprivation on postnatal development of granule cells in the fascia dentata J. Comp. Neurol. 310 1991 356 364
28. C. Escobar, and M. Salas Neonatal undernutrition and amygdaloid nuclear complex development: an experimental study in the rat Exp. Neurol. 122 1993 311 318
29. L.E. Esseveldt, M.N. Van Lehman, and G.J. Boer The suprachiasmatic nucleus and the circadian time-keeping system revisited Brain Res. Rev. 33 2000 34 77
30. W.B. Forbes, C.A. Tracy, O. Resnick, and P.J. Morgane Effect of protein malnutrition during development on sleep behavior of rats Exp. Neurol. 57 1977 440 450
31. Y.A. Fukuda Three-group classification of rat retinal ganglion cells: histological and physiological studies Brain Res. 119 1977 327 344
32. R.C.A. Guedes, A.F.D. Andrade, and J.E. Cabral Filho Propagation of cortical spreading depression in malnourished rats: facilitatory effect of dietary protein deficiency Braz. J. Med. Biol. Res. 20 1987 639 642
33. R.C.A. Guedes, J. Santos-Monteiro, and N.R. Teodósio Malnutrition and brain function; experimental studies using the phenomenon of cortical spreading depression Rev. Brasil. Biol. 56 1996 293 301
34. R.D. Hall, W.B. Forbes, and W.M. Robertson The effects of protein malnutrition on the rat's circadian pattern of food and water intake Nutr. Rep. Int. 18 1978 713 720
35. D.C. Hebert, and R.J. Reiter Influence of protein-caloric malnutrition on the circadian rhythm of pineal melatonin in the rat Proc. Soc. Exp. Biol. Med. 166 1981 360 366
36. T.L. Hickey, and P.F. Hitchcock Genesis of neurons in the dorsal lateral geniculate nucleus of the cat J. Comp. Neurol. 228 1984 186 199
37. G.M. Horsburgh, and A.J. Sefton Cellular degeneration and synaptogenesis in the developing retina of the rat J. Comp. Neurol. 263 1987 553 566
38. A. Hughes The topography of vision in mammals of contrasting life style: comparative optics and retinal organization F. Crescitelli Handbook of Sensory Physiology. The Visual System in Vertebrates vol. VII/5 1977 Springer-Verlag Berlin 613 756
39. Y. Ibata, H. Okamura, M. Tanaka, Y. Tamada, S. Hayashi, N. Iijima, T. Matsuda, K. Munekawa, T. Takamatsu, Y. Hisa, Y. Shigeyoshi, and F. Amaya Functional morphology of the suprachiasmatic nucleus Frontiers Neuroendocrinol. 20 1999 241 268
40. S.M. Innis The role of dietary n-6 and n-3 fatty acids in the developing brain Dev. Neurosci. 22 2000 474 480
41. D.J. Kennaway Programming of the fetal suprachiasmatic nucleus and subsequent adult rhythmicity Trends Endocrinol. Metab. 13 2002 398 402
42. E.S. Lago, N.R. Teodósio, D.C. Pontes Pessoa, and J.E. Cabral Filho Duración de la vida en ratas desnutridas, utilizando dieta básica del nordeste brasileño Arch. Latinoam. Nutr. 47 1997 338 342
43. A.M.O. Leal, and A.C. Moreira Food and the circadian activity of the hypothalamic-pituitary-adrenal axis Braz. J. Med. Biol. Res. 30 1997 1391 1405
44. D.A. Levistsky, and B.J. Strupp Malnutrition and the brain: changing concepts, changing concerns J. Nutr. 125 1995 2212 2220
45. P.D. Lewis, R. Balàzs, A.J. Patel, and A.L. Johnson The effects of undernutrition in early life on cell generation in the rat brain. Brain Res. 893 1975 235 247
46. M.C. Marin, M.E. Tomás, C. Serres, and O. Mercuri Protein-energy malnutrition during gestation and lactation in rats affects growth rate, brain development and essential fatty acid metabolism J. Nutr. 125 1995 1017 1024
47. C.A. Mason, and D.W. Lincoln Visualization of the retino-hypothalamic projection in the rat by cobalt precipitation Cell Tissue Res. 168 1976 117 131
48. M.J. Mc Call, S.R. Robinson, and B. Dreher Differential retinal growth appears to be the primary factor producing the ganglion cell density gradient in the rat Neurosci. Lett. 79 1987 78 84
49. J.P. McAllister II, and G.D. Das Neurogenesis in the epithalamus, dorsal thalamus and ventral thalamus of the rat: an autoradiographic and cytological study J. Comp. Neurol. 172 1977 647 686
50. S. Michell, and C.S. Colwell Cellular communication and coupling within the suprachiasmatic nucleus Chronobiol. Int. 18 2001 579 600
51. R.E. Mistlberger Circadian food-anticipatory activity: formal models and physiological mechanisms Neurosci. Biobehav. Rev. 18 1994 171 195
52. F.M.F. Monteiro, J.A. Albuquerque, and A.M.S. Cabral Influence of a multideficient diet from northeastern Brazil on resting blood pressure and baroreflex sensitivity in conscious, freely moving rats Braz. J. Med. Biol. Res. 34 2001 271 280
53. R.Y. Moore Development of the suprachiasmatic nucleus D.C. Klein R.Y. Moore S.M. Reppert Suprachiasmatic Nucleus. The Mind's Clock 1991 Oxford University Press New York 391 404
54. D.K. Morest The pattern of neurogenesis in the retina of the rat Z. Anat. Entwickl. Gesch. 131 1970 45 67
55. P.J. Morgane, R. Austin-Lafrance, J. Bronzino, J. Tonkiss, S. Diaz-Cintra, L. Cintra, T. Kemper, and J.R. Galler Prenatal malnutrition and development of the brain Neurosci. Biobehav. Rev. 17 1993 91 128
56. P.J. Morgane, M. Miller, T. Kemper, W. Stern, W. Forbes, R. Hall, J. Bronzinno, J. Kissane, E. Hawrylewicz, and O. Resnick The effects of protein malnutrition on the developing central nervous system in the rat Neurosci. Biobehav. Rev. 2 1978 137 230
57. L.P. Morin The circadian visual system Brain Res. Rev. 67 1994 102 127
58. M. Onis, C. de Montiero, J. Akré, and G. Clugston The worldwide magnitude of protein-energy malnutrition: on overview from the WHO global database on child growth Bull. World Health Org. 71 1993 703 712
59. A.D.O. Paixão, F.A. Nunes, J.C. Monteiro, and C.R. Maciel Low sodium chloride content in a multideficient diet induces renal vasodilatation in rats Nutr. Res. 23 2003 85 89
60. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates second edition 1986 Academic Press Inc. California
61. C.W. Picanço-Diniz, M.S. Araújo, J.M.C. Borba, and R.C.A. Guedes NADPH-diaphorase containing neurons and biocytin-labelled axon terminals in the visual cortex of adult rats malnourished during development Nutr. Neurosci. 1 1998 35 48
62. D.C.N. Pontes Pessoa, E.S. de Lago, N.R. Teodósio, and F.M. Bion Dietary proteins on reproductive performance in three consecutive generations of rats Arch. Latinoam. Nutr. 50 2000 55 61
63. O. Rabin, J.-M. Lefauconnier, C. Chanez, G. Bernard, and J.-M. Bourre Developmental effects of intrauterine growth retardation on cerebral amino acid transport Pediatr. Res. 35 1994 640 648
64. B.E. Reese, and R.J. Colello Neurogenesis in the retinal ganglion cell layer of the rat Neuroscience 46 1992 419 429
65. O. Resnick, M. Miller, W. Forbes, R. Hall, T. Kemper, J. Bronzino, and J.P. Morgane Developmental protein malnutrition: influences on the central nervous system of the rat Neurosci. Biobehav. Rev. 3 1979 233 246
66. M. Salas, C. Ruiz, C. Torrero, and S. Pulido Neonatal food restriction: its effects on the sleep cycles and vigil behavior of adult rats Bol. Estud. Méd. Biol. Méx. 32 1983 209 215
67. S.K. Sharma, U. Nayar, M.C. Maheshqari, and B. Singh Effects of undernutrition on developing rat cerebellum: some eletrophysiological and neuromorphological correlates J. Neurol. Sci. 78 1987 261 272
68. N.M. Sherwood, and P.S.A. Timiras Stereotaxic Atlas of the Developing Rat Brain 1970 University of California Press, Ltd. Los Angeles, California
69. R.L. Sidman Histogenesis of the mouse retina studied with thymidine-H3 G.K. Smelser The Structure of the Eye 1961 487 506
70. J.C. Speh, and R.Y. Moore Retinohypothalamic tract development in the hamster and rat Dev. Brain Res. 76 1993 171 181
71. J. Stone A Guide to the Preparation and Analysis of Retinal Whole Mounts 1981 Maitland Publications Pty. Ltd.
72. K. Takatsuji, H. Oyamada, and M. Tohyama Postnatal development of the substance-P, neuropeptide-Y and serotonin-containing fibers in the rat suprachiasmatic nucleus in relation to development of the retinohypothalamic projection Dev. Brain Res. 84 1995 261 270
73. N.R. Teodósio, E.S. Lago, S.A.M. Romani, and R.C.A. Guedes A regional basic diet from northeast Brazil as a dietary model of experimental malnutrition Arch. Latinoam. Nutr. 4 1990 533 547
74. R. Uauy, D.R. Hoffman, P. Peirano, D.G. Birch, and E.E. Birch Essential fatty acids in visual brain development Lipids 36 2001 885 895
75. K.E. Warnes, M.J. Morris, M.E. Symonds, I.D. Phillips, I.J. Clarke, J.A. Owens, and I.C. Mcmillen Effects of increasing gestation, cortisol and maternal undernutrition on hypothalamic neuropeptide Y expression in the sheep fetus J. Neuroendocrinol. 10 1998 51 57
76. D.R. Weaver The suprachiasmatic nucleus: a 25-year retrospective J. Biol. Rhythms 13 1998 100 112
77. C.D. West, and T.L. Kemper The effects of a low protein diet on the anatomical development of the rat brain. Brain Res. 107 1976 221 237