Skip to main content
SpringerLink
Log in

Nerve growth factor restores mRNA levels and the expression of neuropeptides in the suprachiasmatic nucleus of rats submitted to chronic ethanol treatment and withdrawal

  • Published:
Journal of Neurocytology

Abstract

Chronic ethanol treatment and withdrawal from alcohol decrease the synthesis and expression of neuropeptides in the hypothalamic suprachiasmatic nucleus. Given the existing evidence that neurotrophins modulate the synthesis and expression of neurotransmitters/neuromodulators in the mature brain, we have hypothesized that such alterations might result from the reduced biological activity or brain content of neurotrophic factors. To test this possibility, nerve growth factor (NGF) was delivered intraventricularly, over a 4-week period, to rats submitted to ethanol treatment for 6 months and to withdrawn rats. Vasopressin (AVP) and vasoactive intestinal polypeptide (VIP), and the respective mRNAs were detected by immunocytochemistry and in situ hybridization histochemistry, and their levels estimated using stereological methods and densitometry. In ethanol-treated and withdrawn rats, NGF produced increases in the number of AVP- and VIP-immunostained neurons to values identical to those of controls. Corresponding variations were detected in AVP and VIP mRNA levels, which indicates that NGF restored the expression of AVP and VIP by enhancing neuropeptide synthesis. These findings show that NGF can correct the changes induced by chronic ethanol treatment and withdrawal in the gene expression and protein content of the neuropeptides synthesized by suprachiasmatic neurons. They also reveal that NGF plays an important role in the maintenance of the neurochemical phenotype of the suprachiasmatic nucleus in the adult rat. Because suprachiasmatic neurons do not express trkA, NGF might have exerted its effects either through direct signalling of suprachiasmatic neurons via p75NTR activation or, indirectly, by enhancing the activity of the cholinergic and/or glutamatergic afferents to the suprachiasmatic nucleus, or both.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Alfonso, M., DurÁn, R. & MarcÓ, J. (1993) Ethanol-induced alterations in gonadotrophins secretion during the estrous cycle of rats. Alcohol and Alcoholism 28, 667–674.

    Google Scholar 

  • Aloe, L. & Tirassa, P. (1992) The effect of long-term alcohol intake on brain NGF-target cells of aged rats. Alcohol 9, 299–304.

    Google Scholar 

  • Aloe, L., Bracci-Laudiero, L. & Tirassa, P. (1993) The effect of chronic ethanol intake on brain NGF level and on NGF-target tissues of adult mice. Drug and Alcohol Dependence 31, 159–167.

    Google Scholar 

  • Anderson, K. D., Alderson, R. F., Altar, C. A., Distefano, P. S., Corcoran, T. L., Lindsay, R. M. & Wiegand, S. J. (1995) Differential distribution of exogenous BDNF, NGF, and NT-3 in the brain corresponds to the relative abundance and distribution of high-affinity and low-affinity neurotrophin receptors. Journal of Comparative Neurology 357, 296–317.

    Google Scholar 

  • Arendt, T., Henning, D., Gray, J. A. & Marchbanks, R. M. (1988) Loss of neurons in the rat basal forebrain cholinergic projection system after prolonged intake of alcohol. Brain Research Bulletin 21, 563–570.

    Google Scholar 

  • Arendt, T., Allen, Y., Marchbanks, R. M., Schugens, M. M., Sinden, J., Lantos, P. L. & Gray, J. A. (1989) Cholinergic system and memory in the rat: effects of chronic ethanol, embryonic basal forebrain brain transplants and excitotoxic lesions of cholinergic basal forebrain projection system. Neuroscience 33, 435–462.

    Google Scholar 

  • Bear, M. F. & Singer, W. (1986) Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature 320, 172–176.

    Google Scholar 

  • Bina, K. G. & Rusak, B. (1996) Nerve growth factor phase shifts circadian activity rhythms in Syrian hamsters. Neuroscience Letters 206, 97–100.

    Google Scholar 

  • Bina, K. G., Rusak, B. & Semba, K. (1993) Localization of cholinergic neurons in the forebrain and brainstem that project to the suprachiasmatic nucleus of the hypothalamus in rat. Journal of Comparative Neurology 335, 295–307.

    Google Scholar 

  • Bina, K. G., Rusak, B. & Semba, K. (1997) Sources of p75–nerve growth factor receptor-like immunoreactivity in the rat suprachiasmatic nucleus. Neuroscience 77, 461–472.

    Google Scholar 

  • BrandÃo, F., Paula-Barbosa, M. M. & Cadete-Leite, A. (1995) Piracetam impedes hippocampal neuronal loss during withdrawal after chronic alcohol intake. Alcohol 12, 279–288.

    Google Scholar 

  • BrandÃo, F., Cadete-Leite, A., Andrade, J. P., Madeira, M. D. & Paula-Barbosa, M. M. (1996) Piracetam promotes mossy fiber synaptic reorganization in rats withdrawn from alcohol. Alcohol 13, 239–249.

    Google Scholar 

  • BrandÃo, F., Ribeiro-da-Silva, A. & Cadete-Leite, A. (1999) GM1 and piracetam do not revert the alcohol-induced depletion of cholinergic fibers in the hippocampal formation of the rat. Alcohol 12, 279–288.

    Google Scholar 

  • Cadete-Leite, A., BrandÃo, F., Madeira, M. D. & Paula-Barbosa, M. M. (1991) Effects of GM1 ganglioside upon neuronal degeneration during withdrawal from alcohol. Alcohol 8, 417–423.

    Google Scholar 

  • Cadete-Leite, A., Andrade, J. P., Sousa, N., Ma, W. & Ribeiro-da-Silva, A. (1995) Effects of chronic alcohol consumption on the cholinergic innervation of the rat hippocampal formation as revealed by choline acetyltransferase immunocytochemistry. Neuroscience 64, 357–374.

    Google Scholar 

  • Cadete-Leite, A., BrandÃo, F., Andrade, J. P., Ribeiro-da-Silva, A. & Paula-Barbosa, M. M. (1997a) The GABAergic system of the dentate gyrus after withdrawal from chronic alcohol consumption. Effects of intracerebral grafting and putative neuroprotective agents. Alcohol and Alcoholism 32, 471–484.

    Google Scholar 

  • Cadete-Leite, A., BrandÃo, F., Tajrine, D., Antunes, S., Ribeiro-da-Silva, A. & Andrade, J. P. (1997b) Intracerebral grafts promote recovery of the cholinergic innervation of the hippocampal formation in rats withdrawn from chronic alcohol intake. An immunocytochemical study. Neuroscience 79, 383–397.

    Google Scholar 

  • Carnahan, J. & Nawa, H. (1995) Regulation of neuropeptide expression in the brain by neurotrophins. Potential role in vivo. Molecular Neurobiology 10, 135–149.

    Google Scholar 

  • Carter, B. D., Kaltschmidt, C., Kaltschmidt, B., OffenhÄuser, N., BÖhm-Matthaei, R., Baeuerle, P. A. & Bard, Y.-A. (1996) Selective activation of NF-kB by nerve growth factor through the neurotrophin receptor p75. Science 272, 542–545.

    Google Scholar 

  • Chao, M. V. & Hempstead, B. L. (1995) p75 and Trk: a two-receptor system. Trends in Neurosciences 18, 321–326.

    Google Scholar 

  • Colwell, C. S., Kaufman, C. M. & Menaker, M. (1993) Phase-shifting mechanism in the mammalian circadian system: new light on the carbachol paradox. Journal of Neuroscience 13, 1454–1459.

    Google Scholar 

  • Croll, S. D., Wiegand, S. J., Anderson, K. D., Lindsay, R. M. & Nawa, H. (1994) Regulation of neuropeptides in adult rat forebrain by the neurotrophins BDNF and NGF. European Journal of Neuroscience 6, 1343–1353.

    Google Scholar 

  • Daikoku, S., Hisano, S. & Kagotani, Y. (1992) Neuronal associations in the rat suprachiasmatic nucleus demonstrated by immunoelectron microscopy. Journal of Comparative Neurology 325, 559–571.

    Google Scholar 

  • de Witte, P. (1996) The role of neurotransmitters in alcohol dependence: animal research. Alcohol and Alcoholism 31, 13–16.

    Google Scholar 

  • Deimling, M. J. & Schnell, R. C. (1980) Circadian rhythms in the biological response and disposition of ethanol in the mouse. Journal of Pharmacology and Experimental Therapeutics 213, 1–8.

    Google Scholar 

  • Ding, J. M., Chen, D., Weber, E. T., Faiman, L. E., Rea, M. A. & Gillette, M. U. (1994) Resetting the biological clock: mediation of nocturnal circadian shifts by glutamate and NO. Science 266, 1713–1717.

    Google Scholar 

  • Dow, K. E. & Riopelle, R. J. (1985) Ethanol neurotoxicity: effects on neurite formation and neurotrophic factor production in vitro. Science 228, 591–592.

    Google Scholar 

  • Ebling, F. J. P., Maywood, E. S., Staley, K., Humby, T., Hancock, D. C., Waters, C. M., Evan, G. I. & Hastings, M. H. (1991) The role of IN-methyl-D-aspartate-type glutamatergic neurotransmission in the photic induction of immediate-early gene expression in the suprachiasmatic nuclei of the Syrian hamster. Journal of Neuroendocrinology 3, 641–652.

    Google Scholar 

  • Ehlers, M. D., Kaplan, D. R., Price, D. L. & Koliatsos, V. E. (1985) NGF-stimulated retrograde transport of trkA in the mammalian nervous system. Journal of Cell Biology 130, 149–156.

    Google Scholar 

  • Gibbs, R. B. & Pfaff, D. W. (1994) In situ hybridization detection of trkA mRNA in brain: distribution, colocalization with p75NGFR and up-regulation by nerve growth factor. Journal of Comparative Neurology 341, 324–339.

    Google Scholar 

  • Gilliam, D. M. & Collins, A. C. (1983) Circadian and genetic influences on tissue sensitivity and sleep time to ethanol in LS and SS mice. Pharmacology Biochemistry and Behavior 18, 803–808.

    Google Scholar 

  • Gundersen, H. J. G., Jensen, E. B. V., KiÊu, K. & Nielsen, J. (1999) The efficiency of systematic sampling in stereology – reconsidered. Journal of Microscopy 193, 199–211.

    Google Scholar 

  • Heaton, M. B., Swanson, D. J., Paiva, M. & Walker, D. W. (1992) Ethanol exposure affects trophic factor activity and responsiveness in chick embryo. Alcohol 9, 161–166.

    Google Scholar 

  • Heaton, M. B., Paiva, M., Swanson, D. J. & Walker, D. W. (1993) Modulation of ethanol neurotoxicity by nerve growth factor. Brain Research 620, 78–85.

    Google Scholar 

  • Heaton, M. B., Paiva, M., Swanson, D. J. & Walker, D. W. (1994) Responsiveness of cultured septal and hippocampal neurons to ethanol and neurotrophic substances. Journal of Neuroscience Research 39, 305–318.

    Google Scholar 

  • Heaton, M. B., Kim, D. S. & Paiva, M. (2000) Neurotrophic factor protection against ethanol toxicity in rat cerebellar granule cell cultures requires phosphatidylinositol3–kinase activation. Neuroscience Letters 291, 121–125.

    Google Scholar 

  • Hu, L., CÔtÉ, S. L. & Cuello, A. C. (1997) Differential modulation of the cholinergic phenotype of the nucleus basalis magnocellularis neurons by applying NGF at the cell body or cortical terminal fields. Experimental Neurology 143, 162–171.

    Google Scholar 

  • Inouye, S.-I. & Shibata, S. (1994) Neurochemical organization of circadian rhythm in the suprachiasmatic nucleus. Neuroscience Research 20, 109–130.

    Google Scholar 

  • Jacomy, H., Burlet, A. & Bosler, O. (1999) Vasoactive intestinal peptide neurons as synaptic targets for vasopressin neurons in the suprachiasmatic nucleus. Double-label immunocytochemical demonstration in the rat. Neuroscience 88, 859–870.

    Google Scholar 

  • Jarvis, C. R., Xiong, Z. G., Plant, J. R., Churchill, D., Lu, W. Y., Macvicar, B. A. & MacDonald, J. F. (1997) Neurotrophin modulation of NMDA receptors in cultured murine and isolated rat neurons. Journal of Neurophysiology 78, 2363–2371.

    Google Scholar 

  • Kimpinski, K., Jelinski, S. & Mearow, K. (1999) The anti-p75 antibody, MC192, and brain-derived neurotrophic factor inhibit nerve growth factor-dependent neurite growth from adult sensory neurons. Neuroscience 93, 253–263.

    Google Scholar 

  • Kiss, J. & HalÁsz, B. (1996) Synaptic contacts between cholinergic afferents and suprachiasmatic neurons of the rat. NeuroReport 7, 1961–1964.

    Google Scholar 

  • Kiss, J., Patel, A. J. & HalÁsz, B. (1993) Colocalization of NGF receptor with VIP in rat suprachiasmatic neurones. NeuroReport 4, 1315–1318.

    Google Scholar 

  • Klein, D. C., Moore, R. Y. & Reppert, S. M. (1991) Suprachiasmatic Nucleus: The Mind's Clock. New York: Oxford University Press.

    Google Scholar 

  • Koliatsos, V. E., Price, D. L., Gouras, G. K., Cayouette, M. H., Burton, L. E. & Winslow, J. W. (1994) Highly selective effects of nerve growth factor, brain-derived neurotrophic factor, and neurotrophin-3 on intact and injured basal forebrain magnocellular neurons. Journal of Comparative Neurology 343, 247–262.

    Google Scholar 

  • Kume, T., Nishikawa, H., Tomioka, H., Katsuki, H., Akaike, A., Kaneko, S., Maeda, T., Kihara, T. & Shimohama, S. (2000) p75–mediated neuroprotection by NGF against glutamate cytotoxicity in cortical cultures. Brain Research 852, 279–289.

    Google Scholar 

  • Laemle, L. K. (1992) Unilateral enucleation alters vasoactive intestinal polypeptide-like immunoreactivity in the suprachiasmatic nucleus of the rat. Brain Research 572, 325–328.

    Google Scholar 

  • Leal, S., Andrade, J. P., Paula-Barbosa, M. M. & Madeira, M. D. (1998) Arcuate nucleus of the hypothalamus: effects of age and sex. Journal of Comparative Neurology 401, 65–88.

    Google Scholar 

  • Lehman, M. N., Jansen, H. T., Wortman, M., Stevens, P., Kim, C., Norgren, R. B. & Zeitler, P. (1996) Neurotrophin and neurotrophin receptor expression in the suprachiasmatic nucleus (SCN) of rats and hamsters. Society for Neuroscience Abstracts 22, 1141.

    Google Scholar 

  • Lessmann, V. (1998) Neurotrophin-dependent modulation of glutamatergic synaptic transmission in the mammalian CNS. General Pharmacology 31, 667–674.

    Google Scholar 

  • Levin, G. R. & Barde, Y.-A. (1996) Physiology of the neurotrophins. Annual Review of Neuroscience 19, 289–317.

    Google Scholar 

  • Lindsay, R. M. & Harmar, A. J. (1989) Nerve growth factor regulates expression of neuropeptide genes in adult sensory neurons. Nature 337, 362–364.

    Google Scholar 

  • Lindsay, R. M., Wiegand, S. J., Altar, C. A. & Distefano, P. S. (1994) Neurotrophic factors: from molecule to man. Trends in Neurosciences 17, 182–190.

    Google Scholar 

  • Liu, C. & Gillette, M. U. (1996) Cholinergic regulation of the suprachiasmatic nucleus circadian rhythm via a muscarinic mechanism at night. Journal of Neuroscience 16, 744–751.

    Google Scholar 

  • Lovinger, D. M. (1993) Excitotoxicity and alcohol-related brain damage. Alcoholism: Clinical and Experimental Research 17, 19–27.

    Google Scholar 

  • Madeira, M. D., Paula-Barbosa, M. M. (1999) Effects of alcohol on the synthesis and expression of hypothalamic peptides. Brain Research Bulletin 48, 3–22.

    Google Scholar 

  • Madeira, M. D., Andrade, J. P., Lieberman, A. R., Sousa, N., Almeida, O. F. X. & Paula-Barbosa, M. M. (1997) Chronic alcohol consumption and withdrawal do not induce cell death in the suprachiasmatic nucleus, but lead to irreversible depression of peptide immunoreactivity and mRNA levels. Journal of Neuroscience 17, 1302–1319.

    Google Scholar 

  • Mattson, M. P., Lovell, M. A., Furukawa, K. & Markesbery, W. R. (1995) Neurotrophic factors attenuate glutamate-induced accumulation of peroxides, elevation of intracellular Ca2+ concentration, and neurotoxicity and increase antioxidant enzyme activities in hippocampal neurons. Journal of Neurochemistry 65, 1740–1751.

    Google Scholar 

  • Milner, T. A., Wiley, R. G., Kurucs, O. S., Prince, S. R. & Pierce, J. P. (1997) Selective changes in hippocampal neuropeptide Y neurons following removal of the cholinergic septal inputs. Journal of Comparative Neurology 386, 46–59.

    Google Scholar 

  • Mufson, E. J., Kroin, J. S., Sendera, T. J. & Sobreviela, T. (1999) Distribution and retrograde transport of trophic factors in the central nervous system: functional implications for the treatment of neurodegenerative diseases. Progress in Neurobiology 57, 451–484.

    Google Scholar 

  • Nawa, H., Pelleymounter, M. A. & Carnahan, J. (1994) Intraventricular administration of BDNF increases neuropeptide expression in newborn rat brain. Journal of Neuroscience 14, 3751–3765.

    Google Scholar 

  • Nishizawa, M., Hayakawa, Y., Yanaihara, N. & Okamoto, H. (1987) Nucleotide sequence divergence and functional constraint in VIP precursor mRNA evolution between human and rat. FEBS Letters 183, 55–59.

    Google Scholar 

  • Ojeda, S. R., Hill, D. F. & Katz, K. H. (1991) The genes encoding nerve growth factor and its receptor are expressed in the developing female rat hypothalamus. Molecular Brain Research 9, 47–55.

    Google Scholar 

  • Okamura, H., Tanaka, M., Kanemasa, K., Ban, Y., Inouye, S.-I. T. & Ibata, Y. (1994) In situ hibridization histochemistry of vgf mRNA in the rat suprachiasmatic nucleus: co-localization with vasopressin/ neurophysin and VIP/PHI. Neuroscience Letters 182, 181–184.

    Google Scholar 

  • Olson, L., Ayer-Lelievre, C., Ebendal, T., Eriksdotter-Nilsson, M., Ernfors, P., Henschen, A., Hoffer, B., Giacobini, M., Mouton, P., Palmer, M., Persson, H., Sara, V., StrÖmberg, I. & Wetmore, C. (1990) Grafts, growth factors and grafts that make growth factors. Progress in Brain Research 82, 55–66.

    Google Scholar 

  • Paula-Barbosa, M. M., BrandÃo, F., Andrade, J. P., Madeira, M. D., Zimmer, J. & Cadete-Leite, A. (1991) Intracerebral grafting impedes hippocampal cell loss during withdrawal after long-term alcohol consumption in rats. Alcohol and Alcoholism 26, 177–190.

    Google Scholar 

  • Paula-Barbosa, M. M., BrandÃo, F., Madeira, M. D. & Cadete-Leite, A. (1993) Structural changes in the hippocampal formation after long-term alcohol consumption and withdrawal in the rat. Addiction 88, 237–247.

    Google Scholar 

  • Paula-Barbosa, M. M., Andrade, J. P., Cadete-Leite, A. & Madeira, M. D. (2000) NGF increases the synthesis of AVP and VIP in the suprachiasmatic nucleus of rats withdrawn from alcohol. Society for Neuroscience Abstracts 26, 1923.

    Google Scholar 

  • Peterson, D. A., Dickinson-Anson, H. A., Leppert, J. T., Lee, K.-F. & Gage, F. H. (1999) Central neuronal loss and behavioral impairment in mice lacking neurotrophin receptor p75. Journal of Comparative Neurology 404, 1–20.

    Google Scholar 

  • Phillips, S. C. & Cragg, B. G. (1984) Alcohol withdrawal causes a loss of cerebellar Purkinje cells in mice. Journal of Studies on Alcohol 45, 475–480.

    Google Scholar 

  • Rehbein, M., Hillers, M., Mohr, E., Ivell, R., Morley, S., Schmale, H. & Richter, D. (1986) The neurohypophyseal hormones vasopressin and oxytocin: precursor structure, synthesis and regulation. Biological Chemistry 367, 695–704.

    Google Scholar 

  • Rosenberg, M. B., Friedman, T., Robertson, R. C., Tuszynski, M., Wolfe, J. A., Breakefield, X. O. & Gage, F. H. (1988) Grafting genetically modified cells to the damaged brain: restorative effects of NGF expression. Science 242, 1575–1578.

    Google Scholar 

  • Seabold, G. K., Luo, J. & Miller, M. W. (1998) Effect of ethanol on neurotrophin-mediated cell survival and receptor expression in cultures of cortical neurons. Developmental Brain Research 108, 139–145.

    Google Scholar 

  • Segal, R. A. & Greenberg, M. E. (1996) Intracellular signaling pathways activated by neurotrophic factors. Annual Review of Neuroscience 19, 463–489.

    Google Scholar 

  • Semkova, I. & Krieglstein, J. (1999) Neuroprotection mediated via neurotrophic factors and induction of neurotrophic factors. Brain Research Reviews 30, 176–188.

    Google Scholar 

  • Senut, M.-C., Lamour, Y., Lee, J., Brachet, P. & Dicou, E. (1990) Neuronal localization of the nerve growth factor precursor-like immunoreactivity in the rat brain. International Journal of Developmental Neuroscience 8, 65–80.

    Google Scholar 

  • Skup, M. H., Figueiredo, B. C. & Cuello, A. C. (1994) Intraventricular application of BDNF and NT-3 failed to protect nucleus basalis magnocellularis cholinergic neurones. NeuroReport 5, 1105–1109.

    Google Scholar 

  • Sobreviela, T., Clary, D. O., Reichardt, L. F., Brandabur, M. M., Kordower, J. H. & Mufson, E. J. (1994) TrkA-immunoreactive profiles in the central nervous system: colocalization with neurons containing p75 nerve growth factor receptor, choline acetyltransferase, and serotonin. Journal of Comparative Neurology 350, 587–611.

    Google Scholar 

  • Sofroniew, M. V., Isacson, O. & O'Brien, T. S. (1989) Nerve growth factor receptor immunoreactivity in the rat suprachiasmatic nucleus. Brain Research 476, 358–362.

    Google Scholar 

  • Tabakoff, B., Jaffe, R. C. & Ritzmann, R. F. (1978) Corticosterone concentrations in mice during ethanol drinking and withdrawal Journal of Pharmacy and Pharmacology 30, 371–374.

    Google Scholar 

  • Tandrup, T., Gundersen, H. J. G. & Jensen, E. B. V. (1997) The optical rotator. Journal of Microscopy 186, 108–120.

    Google Scholar 

  • Thoenen, H. (1991) The changing scene of neurotrophic factors. Trends in Neurosciences 14, 165–170.

    Google Scholar 

  • Vahlsing, H. L., Varon, S., Hagg, T., Fassholmes, B., Dekker, A., Manley, M. & Manthorpe, M. (1989) An improved device for continuous intraventricular infusions prevents the introduction of pump-derived toxins and increases the effectiveness of NGF treatments. Experimental Neurology 105, 233–243.

    Google Scholar 

  • van den Pol, A. N. & Dudek, F. E. (1993) Cellular communication in the circadian clock: the suprachiasmatic nucleus. Neuroscience 56, 793–811.

    Google Scholar 

  • van den Pol, A. N. & Tsujimoto, K. L. (1985) Neurotransmitters of the hypothalamic suprachiasmatic nucleus: immunocytochemical analysis of 25 neuronal antigens. Neuroscience 15, 1049–1086.

    Google Scholar 

  • van Esseveldt, L. E., Lehman, M. N. & Boer, G. J. (2000) The suprachiasmatic nucleus and the circadian time-keeping system revisited. Brain Research Reviews 33, 34–77.

    Google Scholar 

  • Walker, D. W., Heaton, M. B., Lee, N., King, M. A. & Hunter, B. E. (1993) Effects of chronic ethanol on the septohippocampal system: a role for neurotrophic factors? Alcoholism: Clinical and Experimental Research 17, 12–18.

    Google Scholar 

  • Webb, B., Suarez, S. S., Heaton, M. B. & Walker, D. W. (1997) Cultured postnatal rat septohippocampal neurons change intracellular calcium in response to ethanol and nerve growth factor. Brain Research 778, 354–366.

    Google Scholar 

  • West, M. J., Slomianka, L. & 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. Anatomical Record 231, 482–497.

    Google Scholar 

  • Yoon, S. O., Casaccia-Bonnefil, P., Carter, B. & Chao, M. V. (1998) Competitive signaling between TrkA and p75 nerve growth factor receptors determines cell survival. Journal of Neuroscience 18, 3272–3281.

    Google Scholar 

  • Zhang, Z.-J., Lappi, D. A., Wrenn, C. C., Milner, T. A. & Wiley, R. G. (1998) Selective lesions of the cholinergic basal forebrain causes a loss of cortical neuropeptide Y and somatostatin neurons. Brain Research 800, 198–206.

    Google Scholar 

  • Zhu, X. O. & Waite, P. M. E. (1998) Cholinergic depletion reduces plasticity of barrel field cortex. Cerebral Cortex 8, 63–72.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, Porto Medical School, 4200-319, Porto, Portugal

    Manuel M. Paula-Barbosa, Susana M. Silva, J. Paulo Andrade, António Cadete-Leite & M. Dulce Madeira

Authors
  1. Manuel M. Paula-Barbosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Susana M. Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Paulo Andrade
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. António Cadete-Leite
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Dulce Madeira
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Manuel M. Paula-Barbosa.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Paula-Barbosa, M.M., Silva, S.M., Andrade, J.P. et al. Nerve growth factor restores mRNA levels and the expression of neuropeptides in the suprachiasmatic nucleus of rats submitted to chronic ethanol treatment and withdrawal. J Neurocytol 30, 195–207 (2001). https://doi.org/10.1023/A:1012745606781

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1012745606781

Keywords

Search

Navigation