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The dendritic trees of neurons from the hippocampal formation of protein-deprived adult rats. A quantitative Golgi study

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Abstract

We have recently shown that lengthy periods of low-protein feeding of the adult rat lead to deficits in the number of hippocampal granule and pyramidal cells, and in the number of mossy fiber synapses. These findings prompted us to analyze the dendrites of these neurons to evaluate whether, under the same experimental conditions, degenerative and/or plastic changes also take place at the dendritic level. The hippocampal formations from five 8-month-old rats fed a low-protein diet (casein 8%) for 6 months from the age of 2 months and from five age-matched controls were Golgi-impregnated and the morphology of the dendritic trees quantitatively studied. We found that in malnourished animals there was a reduction in the number of dendritic branches in the dentate granule cells and in the apical dendritic arborizations of CA3 pyramidal neurons. In addition, in the dentate granule cells the spine density was markedly increased and the terminal dendritic segments were elongated in malnourished animals. No alterations were found in the apical dendrites of CA1 pyramidal cells. The results obtained show that long periods of malnutrition induce marked, although not uniform, changes in the dendritic domain of the hippocampal neurons, which reflect the presence of both degenerating and regrowing mechanisms. These alterations are likely to affect the connectivity pattern of the hippocampal formation and, hence, the activity of the neuronal circuitries in which this region of the brain is involved.

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References

  • Altman J, Bayer SA (1990) Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J Comp Neurol 301:365–381

    Google Scholar 

  • Amaral DG, Witter MP (1989) The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31:571–591

    Article  CAS  PubMed  Google Scholar 

  • Andrade JP, Cadete-Leite A, Madeira MD, Paula-Barbosa MM (1991) Long-term low-protein diet reduces the number of hippocampal mossy fiber synapses. Exp Neurol 112:119–124

    Google Scholar 

  • Andrade JP, Madeira MD, Paula-Barbosa MM (1995a) Evidence of reorganization in the hippocampal mossy fiber synapses of adult rats rehabilitated after prolonged undernutrition. Exp Brain Res 104:249–261

    Google Scholar 

  • Andrade JP, Madeira MD, Paula-Barbosa MM (1995b) Effects of long-term malnutrition and rehabilitation on the hippocampal formation of the adult rat. A morphometric study. J Anat 187:379–393

    Google Scholar 

  • Austin K, Bronzino JD, Morgane PJ (1986) Prenatal protein malnutrition affects synaptic potentiation in the dentate gyrus of rats in adulthood. Dev Brain Res 29:267–273

    Google Scholar 

  • Bayer SA (1980) Development of the hippocampal region in the rat. I. Neurogenesis examined with 3H-thymidine autoradiography. J Comp Neurol 190:87–114

    Google Scholar 

  • Bayer SA (1982) Changes in the total number of dentate granule cells in juvenile and adult rats: a correlated volumetric and 3H-thymidine autoradiographic study. Exp Brain Res 46:315–323

    Google Scholar 

  • Bedi KS (1987) Lasting neuroanatomical changes following undernutrition during early life. In: Dobbing J (ed) Early nutrition and later achievement. Academic, London, pp 1–49

    Google Scholar 

  • Brock JW, Prasad C (1992) Alterations in dendritic spine density in the rat brain associated with protein malnutrition. Dev Brain Res 66:266–269

    Google Scholar 

  • Bronzino JD, Austin-LaFrance RJ, Morgane PJ (1990) Effects of prenatal protein malnutrition on perforant path kindling in the rat. Brain Res 515:45–50

    Google Scholar 

  • Bronzino JD, Austin-LaFrance RJ, Morgane PJ, Galler JR (1991) Effects of prenatal protein malnutrition on kindling-induced alterations in dentate granule cell excitability. I. Synaptic transmission measures. Exp Neurol 112:206–215

    Google Scholar 

  • Cáceres A, Busciglio J, Ferreira A, Steward O (1988) An immunocytochemical and biochemical study of the microtubule-associated protein MAP-2 during post-lesion dendritic remodeling in the central nervous system of adult rats. Mol Brain Res 3:233–246

    Google Scholar 

  • Cadete-Leite A, Tavares MA, Uylings HBM, Paula-Barbosa M (1988) Granule cell loss and dendritic regrowth in the hippocampal dentate gyrus of the rat after chronic alcohol consumption. Brain Res 473:1–14

    Google Scholar 

  • Cadete-Leite A, Tavares MA, Alves MC, Uylings HBM, Paula-Barbosa MM (1989) Metric analysis of hippocampal granule cell dendritic trees after alcohol withdrawal in rats. Alcohol Clin Exp Res 13:837–840

    Google Scholar 

  • Castro CA, Tracy M, Rudy JW (1989) 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 32:255–264

    Google Scholar 

  • Cintra L, Díaz-Cintra S, Galván A, Kemper T, Morgane PJ (1990) Effects of protein undernutrition on the dentate gyrus in rats of three age groups. Brain Res 532:217–277

    Google Scholar 

  • Coleman PD, Flood DG (1986) Dendritic proliferation in the aging brain as a compensatory repair mechanism. Prog Brain Res 70:227–237

    Google Scholar 

  • Coleman PD, Riesen AH (1968) Environmental effects on cortical dendritic fields. I. Rearing in the dark. J Anat 102:363–374

    Google Scholar 

  • Cordero ME, Trejo M, García E, Barros T, Colombo M (1985) Dendritic development in the neocortex of adult rats subjected to postnatal malnutrition. Early Hum Dev 12:309–321

    Google Scholar 

  • Cotman CW, Nadler JV (1978) Reactive synaptogenesis in the hippocampus. In: Cotman CW (ed) Neuronal plasticity. Raven, New York, pp 227–271

    Google Scholar 

  • De Ruiter JP, Uylings HBM (1987) Morphometric and dendritic analysis of fascia dentata granule cells in human aging and senile dementia. Brain Res 402:217–229

    Google Scholar 

  • De Voogd TJ, Chang FLF, Floeter MK, Jencius MJ, Greenough WT (1981) Distortions induced in neuronal quantification by camera lucida analysis: comparisons using a semi-automated data acquisition system. J Neurosci Methods 3:285–294

    Google Scholar 

  • Desmond NL, Levy WB (1985) Granule cell dendritic spine density in the rat hippocampus varies with spine shape and location. Neurosci Lett 54:219–224

    Google Scholar 

  • Díaz-Cintra S, Cintra L, Kemper T, Resnick O, Morgane PJ (1981) The effects of protein deprivation on the nucleus raphe dorsalis: a morphometric Golgi study in rats of three age groups. Brain Res 221:243–255

    Google Scholar 

  • Diaz-Cintra S, Cintra L, Kemper T, Resnick O, Morgane PJ (1984) The effects of protein deprivation on the nucleus locus coeruleus: a morphometric Golgi study in rats of three age groups. Brain Res 304:243–253

    Google Scholar 

  • Díaz-Cintra S, Cintra L, Ortega A, Kemper T, Morgane PJ (1990) Effects of protein deprivation on pyramidal cells of the visual cortex in rats of three age groups. J Comp Neurol 292:117–126

    Google Scholar 

  • Díaz-Cintra S, Cintra L, Galván A, Aguilar A, Kemper T, Morgane PJ (1991) Effects of prenatal protein deprivation on postnatal development of granule cells in the fascia dentata. J Comp Neurol 310:356–364

    Google Scholar 

  • Dobbing J (1968) Vulnerable periods in developing brain. In: Davidson AN, Dobbing J (eds) Applied neurochemistry. Davis, Philadelphia, pp 287–316

    Google Scholar 

  • Eayrs TJ (1955) The cerebral cortex of normal and hypothyroid rats. Acta Anat 25:160–183

    Google Scholar 

  • Eckenhoff MF, Rakic R (1984) Radial organization of the hippocampal dentate gyrus: a Golgi, ultrastructural and immunocytochemical analysis in the developing Rhesus monkey. J Comp Neurol 223:1–21

    Google Scholar 

  • Feldman ML, Peters A (1979) A technique for estimating total spine numbers on Golgi-impregnated dendrites. J Comp Neurol 188:527–542

    Google Scholar 

  • Fitch JM, Juraska JM, Washington LW (1989) The dendritic morphology of pyramidal neurons in the rat hippocampal CA3 area. I. Cell types. Brain Res 479:105–114

    Google Scholar 

  • Flood DG, Buell SJ, Horwitz GJ, Coleman PD (1987) Dendritic extent in human dentate gyrus granule cells in normal aging and senile dementia. Brain Res 402:205–216

    Google Scholar 

  • García-Ruiz M, Díaz-Cintra S, Cintra L, Corkidi G (1993) Effect of protein malnutrition on CA3 hippocampal pyramidal cells in rats of three ages. Brain Res 625:203–212

    Google Scholar 

  • Gould E, Westlind-Danielsson A, Frankfurt M, McEwen BS (1990) Sex differences and thyroid hormone sensitivity of hippocampal pyramidal cells. J Neurosci 10:996–1003

    Google Scholar 

  • Green EJ, Juraska JM (1985) The dendritic morphology of hippocampal dentate granule cells varies with their position in the granule cell layer: a quantitative Golgi study. Exp Brain Res 59:582–586

    Google Scholar 

  • Hammer RP Jr (1981) The influence of pre-and postnatal undernutrition on the developing brain stem reticular core: a quantitative Golgi study. Dev Brain Res 1:191–201

    Google Scholar 

  • Horner CH (1993) Plasticity of the dendritic spine. Prog Neurobiol 41:281–321

    Google Scholar 

  • Horwitz B (1981) Neuronal plasticity: how changes in dendritic architecture can affect the spread of postsynaptic potentials. Brain Res 224:412–418

    Google Scholar 

  • Jacobs B, Scheibel AB (1993) A quantitative dendritic analysis of Wernicke's area in humans. I. Lifespan changes. J Comp Neurol 327:83–96

    Google Scholar 

  • Leuba G, Rabinowicz T (1979) Long-term effects of postnatal undernutrition and maternal malnutrition on mouse cerebral cortex. II. Evolution of dendritic branchings and spines in the visual region. Exp Brain Res 37:299–308

    Google Scholar 

  • Madeira MD, Sousa N, Lima-Andrade MT, Calheiros F, Cadete-Leite A, Paula-Barbosa MM (1992) Selective vulnerability of the hippocampal pyramidal neurons to hypothyroidism in male and female rats. J Comp Neurol 322:501–518

    Google Scholar 

  • McConnell P (1980) Nutritional effects on non-mitotic aspects of central nervous system development. Prog Brain Res 53:99–108

    Google Scholar 

  • McMullen PA, Saint-Cyr JA, Carlen PL (1984) Morphological alterations in rat CA1 hippocampal pyramidal cell dendrites resulting from chronic ethanol consumption and withdrawal. J Comp Neurol 225:111–118

    Google Scholar 

  • Moore DS, McCabe GP (1989) Introduction to the practice of statistics. Freeman, New York

    Google Scholar 

  • Morgane PJ, Miller M, Kemper T, Stern W, Forbes W, Hall R, Bronzino J, Kissane J, Hawrylewicz E, Resnick O (1978) The effects of protein malnutrition on the developing central nervous system in the rat. Neurosci Biobehav Rev 2:137–230

    CAS  PubMed  Google Scholar 

  • Morgane PJ, Austin-LaFrance RJ, Bronzino JD, Tonkiss J, Galler JR (1992) Malnutrition and the developing central nervous system. In: Isaacson RL, Jensen KF (eds) The vulnerable brain and environmental risks. (Malnutrition and hazard assessment, vol 1) Plenum, New York, pp 3–44

    Google Scholar 

  • Morgane PJ, Austin-LaFrance R, Bronzino J, Tonkiss J, Díaz-Cintra S, Cintra L, Kemper T, Galler JR (1993) Prenatal malnutrition and development of the brain. Neurosci Biobehav Rev 17:91–128

    Google Scholar 

  • Noback CR, Eisenman LM (1981) Some effects of protein-calorie undernutrition on the developing central nervous system of the rat. Anat Rec 201:67–73

    Google Scholar 

  • Palay SL, Chan-Palay V (1974) Cerebellar cortex. Cytology and organization. Springer, Berlin Heidelberg New York, pp 322–336

    Google Scholar 

  • Paula-Barbosa MM, Andrade JP, Castedo JL, Azevedo FP, Camões I, Volk B, Tavares MA (1989) Cell loss in the cerebellum and hippocampal formation of adult rats after long-term low-protein diet. Exp Neurol 103:186–193

    Google Scholar 

  • Pentney RJ (1995) Measurements of dendritic path lengths provide evidence that ethanol-induced lengthening of terminal dendritic segments may result from dendritic regression. Alcohol Alcohol 30:87–96

    Google Scholar 

  • Pyapali GK, Turner DA (1994) Denervation-induced dendritic alterations in CA1 pyramidal cells following kainic acid hippocampal lesions in rats. Brain Res 652:279–290

    Google Scholar 

  • Rami A, Patel AJ, Rabié A (1986) Thyroid hormone and development of the rat hippocampus: morphological alterations in granule and pyramidal cells. Neuroscience 19:1217–1226

    Google Scholar 

  • Salas M, Díaz S, Nieto A (1974) Effects of neonatal food deprivation on cortical spines and dendritic development of the rat. Brain Res 73:139–144

    Google Scholar 

  • Schadé JP, Baxter CF (1960) Changes during growth in the volume and surface area of cortical neurons in the rabbit. Exp Neurol 2:158–178

    Google Scholar 

  • Schönheit B, Haensel P (1984) Effect of nonspecific malnutrition on spine morphology of lamina V pyramidal cells of the cingulate area of juvenile and adult rats. J Hirnforsch 25:617–631

    Google Scholar 

  • Sotelo C (1975) Anatomical, physiological and biochemical studies of the cerebellum from mutant mice. II. Morphological study of cerebellar cortical neurons and circuits in the weaver mouse. Brain Res 94:19–44

    Google Scholar 

  • Sotelo C, Privat A (1978) Synaptic remodeling of the cerebellar circuitry in mutant mice and experimental cerebellar malformations. Study “in vivo” and “in vitro”. Acta Neuropathol 43:19–34

    Google Scholar 

  • Stensaas LJ (1967) The development of hippocampal and dorsolateral pallial regions of the cerebral hemisphere in fetal rabbits. I. Fifteen millimeter stage, spongioblast morphology. J Comp Neurol 129:59–70

    Google Scholar 

  • Steward O (1987) Regulation of synaptogenesis through the local synthesis of proteins at the postsynaptic site. Prog Brain Res 71:267–279

    Google Scholar 

  • Tavares MA, Paula-Barbosa MM, Gray EG (1983) Dendritic spine plasticity and chronic alcoholism in rats. Neurosci Lett 42:235–238

    Google Scholar 

  • Thoenen H (1991) The changing scene of neurotrophic factors. Trends Neurosci 14:165–170

    Article  CAS  PubMed  Google Scholar 

  • Tonkiss J, Galler JR (1990) Prenatal protein malnutrition and working memory performance in adult rats. Behav Brain Res 40:95–107

    Google Scholar 

  • Trommald M, Jensen V, Andersen P (1995) Analysis of dendritic spines in rat CA1 pyramidal cells intracellularly filled with a fluorescent dye. J Comp Neurol 353:260–274

    Google Scholar 

  • Uemura E, Carriquiry A, Kliemann W, Goodwin J (1995) Mathematical modeling of dendritic growth in vitro. Brain Res 671:187–194

    Google Scholar 

  • Uylings HBM, Smit GJ, Veltman WAM (1975) Ordering methods in quantitative analysis of branching structures of dendritic trees. In: Kreutzberg GW (ed) Adv Neurol 12:247–254

  • Uylings HBM, Ruiz-Marcos A, van Pelt J (1986) The metric analysis of three-dimensional dendritic tree patterns: a methodological review. J Neurosci Methods 18:127–151

    Google Scholar 

  • Warren MA, Freestone T, Thomas AJ (1989) Undernutrition during early adult life significantly affects neuronal connectivity in rat visual cortex. Exp Neurol 103:290–292

    Google Scholar 

  • West CD, Kemper TL (1976) The effects of a low protein diet on the anatomical development of the rat brain. Brain Res 107:221–237

    Google Scholar 

  • Woolley CS, McEwen BS (1993) Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J Comp Neurol 336:293–306

    Google Scholar 

  • Woolley CS, Gould E, McEwen BS (1990) Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res 531:225–231

    Google Scholar 

  • Yamada M, Wada Y, Tsukagoshi H, Otomo E-I, Hayakawa M (1988) A quantitative Golgi study of basal dendrites of hippocampal CA1 pyramidal cells in senile dementia of Alzheimer type. J Neurol Neurosurg Psychiatry 51:1088–1090

    Google Scholar 

  • Zimmer J, Laurberg S, Sunde N (1983) Neuroanatomical aspects of normal and transplanted hippocampal tissue. In Seifert W (ed) Neurobiology of the hippocampus. Academic, London, pp 39–64

    Google Scholar 

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Andrade, J.P., Castanheira-Vale, A.J., Paz-Dias, P.G. et al. The dendritic trees of neurons from the hippocampal formation of protein-deprived adult rats. A quantitative Golgi study. Exp Brain Res 109, 419–433 (1996). https://doi.org/10.1007/BF00229626

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