Publication Cover
Nutritional Neuroscience
An International Journal on Nutrition, Diet and Nervous System
Volume 2, 1999 - Issue 4
13
Views
6
CrossRef citations to date
0
Altmetric
Original Articles

Effect of Prenatal Protein Malnutrition on Birthdates and Number of Neurons in the Rat Locus Coeruleus

, , , , , & show all
Pages 267-276 | Received 15 Feb 1999, Published online: 13 Jul 2016

References

  • Almeida, S.S., Tonkiss, J. and Galler, J.R. (1996a) Prenatal protein malnutrition affects the social interactions of juvenile rats. Physiol. Behav. 60, 197–201.
  • Almeida, S.S., Tonkiss, J. and Galler, J.R. (1996b) Prenatal protein malnutrition affects exploratory behavior of female rats in the elevated plus maze. Physiol Behav. 60, 675–680.
  • Almeida, S.S., Tonkiss, J. and Galler, J.R. (1996c) Prenatal protein malnutrition affects avoidance but not escape behavior in the elevated T-maze test. Physiol. Behav. 60, 191–195.
  • Altman, J. and Bayer, S. (1980) Development of the brain stem in the rat. IV. Thymidine-radiographic study of the time of origin of neurons in the pontine region. J. Comp. Neurol. 194, 905–929.
  • Barnes, D. and Altman, J. (1973a) Effects of different schedules of early undemutrition on the preweaning growth of the rat cerebellum. Exp. Neurol. 38, 406–419.
  • Barnes, D. and Altman, J. (1973b) Effects of two levels of gestational-lactational undernutrition on the postweaning growth of the rat cerebellum. Exp. Neurol. 38, 420–428.
  • Bass, N.H., Netsky, M.G. and Young, E. (1970) Effect of neonatal malnutrition on developing cerebrum. I. Microchemical and histological study of cellular differentiation in the rat. Arch. Neurol. 23, 289–302.
  • Bayer, S.A. (1980) Development of the hippocampal region in the rat II. Neurogenesis examined with 3H-thymidine autoradiography. J. Comp. Neurol. 190, 87–114.
  • Bayer, S.A. and Altman J. (1974) Hippocampal development in the rat: Cytogenesis and morphogenesis examined with autoradiography and low-level X-irradiation. J. Comp. Neurol. 158, 50–80.
  • Blatt, G.J., Chen, J.C., Rosene, D.L., Volicer, L. and Galler, J.R. (1994) Prenatal protein malnutrition effects on the serotonergic system in the hippocampal formation: an immunocytochemical, ligand binding, and neurochemical study. Brain Res. Bull. 34, 507–518.
  • Blue, M.E. and Parnavelas, J.G. (1982) The effect of neonatal 6-hydroxydopamine treatment on synaptogenesis in the visual cortex of the rat. J. Comp. Neurol. 205, 199–205.
  • Brenner, E., Mirmiran, M., Uylings, H.B. and Van der Gugten, J. (1983) Impaired growth of the cerebral cortex of rats treated neonatally with 6-hydroxydopamine under different environmental conditions. Neurosci. Lett. 42, 13–17.
  • Bronzino, J.D., Austin-LaFrance, R.J., Morgane, P.J. and Galler, J.R. (1991a) Effects of prenatal protein malnutrition on kindling-induced alterations in dentate granule cell excitability. I. Synaptic transmission measures. Exp. Neurol. 112, 206–215.
  • Bronzino, J.D., Austin-LaFrance, R.J., Morgane, P.J. and Galler, J.R. (1991b) Effects of prenatal protein malnutrition on kindling-induced alterations in dentate granule cell excitability. II. Paired pulse measures. Exp. Neurol. 112, 216–223.
  • Bronzino, J.D., Blaise, J.H., Mokler, D.J. and Morgane, P.J. (1997) Effects of prenatal protein malnutrition on hippocampal long term potentiation in freely moving rats. Exp. Neurol. 148, 317–323.
  • Bronzino, J.D., Austin-LaFrance, R.J., Mokler, D.J., Galler, J.R. and Morgane, P.J. (1999) Modulation of paired-pulse responses in the dentate gyrus: Part II. Effects of prenatal protein malnutrition. Hippocampus (in press).
  • Cintra, L., Aquilar, A., Granados, L., Galván, A., Kemper, T., DeBassio, W., Galler, J., Morgane, P, Durán, P. and Díaz-Cintra, S. (1997a) Effects of prenatal protein malnutrition on CA1 pyramidal cells in rats of four ages. Hippocampus 7, 192–203.
  • Cintra, L., Díaz-Cintra, S., Galván, A., Kemper, T.L. and Morgane, P.J. (1990) Effect of protein undernutrition on the dentate gyrus in rats of three age groups. Brain Res. 532, 271–277.
  • Cintra, L., Díaz-Cintra, S., Kemper, T. and Morgane, P.J. (1982) Nucleus locus coeruleus: a morphometric Golgi study in rats of three age groups. Brain Res. 247, 17–28.
  • Cintra, L., Granados, L., Aguilar, A., Kemper, T., DeBassio, W., Galler, J., Morgane, P, Durán, P. and Díaz-Cintra, S. (1997b) Effects of prenatal protein malnutrition on mossy fibers of the hippocampal formation in rats of four age groups. Hippocampus 7, 184–191.
  • DeBassio, W.A. and Kemper, T.L. (1985) The effects of protein deprivation on neuronal migration in rats. Develop. Brain Res. 20, 191–196.
  • DeBassio, W.A., Kemper, T.L., Galler, J.R. and Tonkiss, J. (1994) Prenatal malnutrition effect on pyramidal and granule cell generation in the hippocampal formation. Brain Res. Bull. 35, 57–61.
  • DeBassio, W.A., Kemper, T.L., Tonkiss, J. and Galler, J.R. (1996) Effect of prenatal protein deprivation on postnatal granule cell generation in the hippocampal dentate gyrus. Brain Res. Bull. 41, 379–383.
  • Del Rio, J.A. and Soriano, E. (1989) Immunocytochemical detection of 5′-bromodeoxyuridine incorporation in the central nervous system of the mouse. Dev. Brain Res. 49, 311–317.
  • Díaz-Cintra, S., Cintra, L., Galván, A., Aguilar, A., Kemper, T.L. and Morgane, P.J. (1991) Effects of prenatal protein deprivation on postnatal development of granule cells in the fascia dentata. J. Comp. Neurol. 310, 356–364.
  • Díaz-Cintra, S., Cintra, L., Kemper, T.L., Resnick, O. and Morgane, P.J. (1984) The effects of protein deprivation on the locus coeruleus: a morphometric Golgi study in rats of three age groups. Brain Res. 304, 243–253.
  • Díaz-Cintra, S., García-Ruiz, M., Corkidi, G. and Cintra, L. (1994) Effects of prenatal malnutrition and postnatal nutritional rehabilitation on CA3 hippocampal pyramidal cells in rats of four ages. Brain Res. 662, 117–126.
  • Dobbing, J., Hopewell, J.W. and Lynch, A. (1971) Vulnerability of developing brain: VII. Permanent deficit of neurons in the cerebral and cerebellar cortex following early mild undemutrition. Exp. Neurol. 32, 439–447.
  • Galler, J.R., Shumsky, J.S. and Morgane, P.J. (1996) Malnutrition and brain development. In: Walker, C.A. and Watkins, J.B. (Eds.), Nutrition in Pediatrics: Basic Science and Clinical Applications, 2nd edn. (Neuilly-sur-Seine, France: Decker Europe, Inc.), pp. 196–212.
  • Galler, J.R. and Tonkiss, J. (1991) Prenatal protein malnutrition and maternal behavior in Sprague-Dawley rats. J. Nutr. 121, 762–769.
  • Galler, J.R., Tonkiss, J. and Maldonado-Irizarry, C.S. (1994) Prenatal protein malnutrition and home orientation in the rat. Physiol. Behav. 55, 993–996.
  • Gressens, P., Muaku, S.M., Besse, L., Nsegbe, E., Gallego, J., Delpech, B., Gaultier, C., Evrard, P, Ketelslegers, J. and Maiter, D. (1997) Maternal protein restriction early in rat pregnancy alters brain development in the progeny. Dev. Brain Res. 103, 21–35.
  • Kaplan, M.S. and Hinds, J.W. (1977) Neurogenesis in the adult rat: Electron microscopic analysis of light radioautographs. Science 197, 1092–1094.
  • Katz, H.B. and Davies, C.A. (1982) The effects of early-life undernutrition and subsequent environment on morphological parameters of the rat brain. Behav. Brain Res. 5, 53–64.
  • Katz, H.B. and Davies, C.A. (1983) The separate and combined effects of early undemutrition and environmental complexity at different ages on cerebral measures in rats. Dev. Psychobiol. 16, 47–58.
  • Katz, H.B., Davies, C.A. and Dobbing, J. (1982) The effects of undernutrition at different ages early in life and later environmental complexity on parameters of the cerebrum and hippocampus in rats. J. Nutrit. 112, 1362–1368.
  • Kolb, B. and Sutherland, R.J. (1992) Noradrenaline depletion blocks behavioral sparing and alters cortical morphogenesis after neonatal frontal cortex damage in rats. J. Neurosci. 12, 2321–2330.
  • Lauder, J.M. and Bloom, F.E. (1974) Ontogeny of monoamine neurons in the locus coeruleus, raphe nuclei and substantia nigra of the rat. I. cell differentiation. J. Comp. Neurol. 155, 469–482.
  • Lewis, P.D., Patel, A.J. and Belazs, R. (1979) Effect of undernutrition on cell generation in the rat hippocampus. Brain Res. 168, 186–189.
  • Lewis, P.D., Balazs, R., Patel, A.J. and Johnson, A.L. (1975) The effects of undernutrition in early life on cell generation in the rat brain. Brain Res. 83, 235–247.
  • Lindvall, O. and Bjørklund, A. (1983) Dopamine- and norepinephrine-containing neuron systems: Their anatomy in the rat brain. In: Emson, G. (Ed.), Chemical Neuroanatomy (New York: Raven Press), pp. 229–255.
  • Loy, R., Koziell, D., Lindsey, J. and Moore, R.Y. (1980) Noradrenergic innervation of the adult rat hippocampal formation. J. Comp. Neurol. 189, 699–710.
  • Marín-Padilla, M. (1978) Dual origin of the mammalian neocortex and evolution of the cortical plate. Anat. Embryol. 152, 109–126.
  • Miller, M.W. and Nowakowski, R.S. (1988) Use of bromo-deoxyuridine-immunohistochemistry to examine the proliferation, migration and time of origin of cells in the central nervous system. Brain Res. 457, 44–52.
  • Molliver, M.E. (1982) Role of monoamine in the development of the neocortex. Neurosci. Res. Bull. Prog. 20, 492–507.
  • Morgane, P.J., Austin-LaFrance, R., Bronzino, J., Tonkiss, J., Díaz-Cintra, S., Cintra, L., Kemper, T. and Galler, J.R. (1993) Prenatal malnutrition and development of the brain. Neurosci. Biobehav. Rev. 17, 91–128.
  • Nowakowski, R.S., Lewin, S.B. and Miller, M.W. (1989) Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J. Neurocytol. 18, 311–318.
  • Paxinos, G. and Watson, C. (1986) The Rat Brain in Stereotactic Coordinates. 2nd edn. Sydney: Academic Press.
  • Raedler, E., Raedler, A. and Feldhaus, S. (1980) Dynamic aspects of neocortical ontogenesis in the rat. Anat. Embryol. 158, 253–269.
  • Resnick, O., Miller, M., Forbes, W.B., Hall, R., Kemper, T., Bronzino, J. and Morgane, P.J. (1979) Developmental protein malnutrition: Influences on the central nervous system of the rat. Neurosci. Biobehav. Rev. 3, 233–246.
  • Sima, A. and Persson, L. (1975) The effect of pre- and postnatal undernutrition on the development of the rat cerebellar cortex. Neurobiol. 5, 23–34.
  • Soriano, E. and Del Rio, J.A. (1991) Simultaneous immunocytochemical visualization of bromodeoxyuridine and neural tissue antigens. J. Histochem. Cytochem. 39, 255–263.
  • Stern, W.C., Miller, M., Forbes, W.B., Morgane, P.J. and Resnick, O. (1975) Ontogeny of the levels of biogenic amines in various parts of the brain and in peripheral tissues in normal and protein malnourished rats. Exp. Neurol. 49, 314–326.
  • Tonkiss, J., Galler, J.R., Shukitt-Hale, B. and Rocco, F.J. (1991) Prenatal protein malnutrition impairs visual discrimination learning in adult rats. Psychobiology 19, 247–250.
  • Tonkiss, J., Harrison, R.H. and Galler, J.R. (1996) Differential effects of prenatal protein malnutrition and prenatal cocaine on a test of homing behavior in rat pups. Physiol. Behav. 60, 1013–1018.
  • Wallingford, J.C., Shrader, R.E. and Zeman, F.J. (1980) Effect of maternal protein-calorie malnutrition on fetalrat cerebellar neurogenesis. J. Nutr. 110, 543–551.
  • West, M.J. (1993) New stereological methods for counting neurons. Neurobiol. Aging 14, 275–285.
  • West, M.J. and Gundersen, H.J.G. (1990) Unbiased stereological estimation of the number of neurons in the human hippocampus. J. Comp. Neurol. 296, 1–22.
  • West, M.J., Østergaard, K., Andreassen, O.A. and Finsen, B. (1996) Estimation of the number of somatostatin neurons in the striatum: an in situ hybridization study using the optical fractionator method. J. Comp. Neurol. 370, 11–22.
  • West, M.J., Slomianka, L. and Gundersen, H.J.G. (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat. Rec. 231, 482–497.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.