Hostname: page-component-7dd5485656-wlg5v Total loading time: 0 Render date: 2025-10-30T18:22:24.226Z Has data issue: false hasContentIssue false
  • English
  • Français

Nerve growth factor (NGF) uptake and transport following injection in the developing rat visual cortex

Published online by Cambridge University Press:  02 June 2009

Luciano Domenici ,
Gigliola Fontanesi ,
Antonio Cattaneo ,
Paola Bagnoli  and
Lamberto Maffei
Luciano Domenici
Affiliation:
Institute of Neurophysiology, Italian Research Council, Pisa, Italy
Gigliola Fontanesi
Affiliation:
Department of Physiology and Biochemistry, University of Pisa, Italy
Antonio Cattaneo
Affiliation:
International School of Advanced Studies, University of Trieste, Italy
Paola Bagnoli
Affiliation:
Department of Physiology and Biochemistry, University of Pisa, Italy
Lamberto Maffei
Affiliation:
Institute of Neurophysiology, Italian Research Council, Pisa, Italy
Get access Rights & Permissions [Opens in a new window]

Abstract

Recent investigations have shown that cortical nerve growth factor (NGF) infusions during the critical period inhibit ocular-dominance plasticity in the binocular portion of the rat visual cortex. The mechanisms underlying the effects of NGF on visual cortical plasticity are still unclear. To investigate whether during normal development intracortical and/or extracortical cells possess uptake/transport mechanisms for the neurotrophin, we injected 125I-NGF into the occipital cortex of rats at different postnatal ages. Within the cortex, only a few labelled cells were observed. These cells were confined to the vicinity of the injection site and their number depended on the animal's age at the time of injection. Labelled cells were absent at postnatal day (PD) 10 but could be detected between PD 14 and PD 18. They then decreased in number over the following period and were not detected in adult animals. Outside the cortex, neurons of the lateral geniculate nucleus (LGN) were not observed to take up and retrogradely transport NGF at any age after birth. In contrast, retrogradely labelled neurons were found in the basal forebrain. Labelled cells were first observed here at PD 14 and then increased in number until reaching the adult pattern. Our results show that intrinsic and extrinsic neurons are labelled following intracortical injections of iodinated NGF. In both neuronal populations, the uptake and transport of NGF is present over a period corresponding to the critical period for visual cortical plasticity. These findings suggest that NGF may play a role, both intra and extracortically, in plasticity phenomena.

Keywords

NeurotrophinVisual cortexBasal forebrainLateral geniculate nucleusDevelopmentPlasticity

Information

Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 6 , November 1994 , pp. 1093 - 1102
Copyright
Copyright © Cambridge University Press 1994

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Allendoerfer, K.L., Shelton, D.L., Shooter, E.M. & Shatz, C.J. (1990). Nerve growth factor receptor immunoreactivity is transiently associated with the subplate neurons of the mammalian cerebral cortex. Proceedings of the National Academy of Sciences of the U.S.A. 87, 187–190.CrossRefGoogle ScholarPubMed
Araujo, D.M., Chabot, J.G. & Quirion, T. (1990). Potential neuro-trophic factors in the mammalian central nervous system: Functional significance in the developing and aging brain. International Reviews in Neurobiology 32, 141–174.CrossRefGoogle Scholar
Bagnoli, P., Fontanesi, G., Streit, P., Domenici, L. & Alesci, R. (1989). Changing distribution of GABA-like immunoreactivity in pigeon visual areas during the early posthatching period and the effects of retina removal on tectal GABAergic systems. Visual Neuroscience 3, 491–508.CrossRefGoogle ScholarPubMed
Bagnoli, P., Fontanesi, G., Alesci, R. & Erichsen, J.T. (1992). Distribution of neuropeptide Y, substance P and choline acetyltransferase in the developing visual system of the pigeon and effects of unilateral retina removal. Journal of Comparative Neurology 3, 392–414.CrossRefGoogle Scholar
Bear, M.F. & Singer, W. (1986). Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature 320, 172–176.CrossRefGoogle ScholarPubMed
Berardi, N., Domenici, L., Parisi, V., Plzzorusso, T., Cellerino, A. & Maffei, L. (1993). Monocular deprivation effects in the rat visual cortex and lateral geniculate nucleus are prevented by nerve growth factor (NGF). I. Visual cortex. Proceedings of the Royal Society B (London) 251, 17–23.Google ScholarPubMed
Berardi, N., Cellerjno, A., Domenici, L., Fagiolini, M., Cattaneo, A. & Maffei, L. (1994). Monoclonal antibodies to nerve growth factor affect the postnatal development of the visual system. Proceedings National Academy of Sciences of the U.S.A. 91, 684–688.CrossRefGoogle ScholarPubMed
Berninger, B., Garcia, D.E., Inagaki, N., Hahnel, C. & Lindholm, D. (1993). BDNF and NT-3 induce intracellular Ca2+ elevation in hippocampal neurones. NeuroReport 4, 1303–1306.CrossRefGoogle ScholarPubMed
Bocchini, V. & Angeletti, P.U. (1969). The nerve growth factor: Purification as a 30,000-molecular-weight protein. Proceedings of the National Academy of Sciences of the U.S.A. 64, 787–794.CrossRefGoogle ScholarPubMed
Bozzi, Y., Pizzorusso, T., Cremisi, F., Comelli, M.C., Berardi, N. & Maffei, L. (1993). Monocular deprivation decreases the expression of BDNF mRNA in the rat visual cortex. Society for Neuro-science Abstracts 19, 8.7.Google Scholar
Carey, R.G. & Rieck, R.W. (1987). Topographic projections to the visual cortex from the basal forebrain in the rat. Brain Research 424, 205–215.CrossRefGoogle Scholar
Carmignoto, G., Canella, R., Candeo, P., Comelli, M.C. & Maffei, L. (1993 a). Effects of nerve growth factor on neuronal plasticity of the kitten visual cortex. Journal of Physiology 464, 343–360.CrossRefGoogle ScholarPubMed
Carmignoto, G., Negro, A. & Vicini, S. (1993 b). NGF and BDNF modulate excitatory synapses in rat visual cortical neurons. Society for Neuroscience Abstracts 19, 690.9.Google Scholar
Castren, E., Zafra, F., Thoenen, H. & Lindholm, D. (1992). Light regulates expression of brain-derived neurotrophic factor mRNA in rat visual cortex. Proceedings of the National Academy of Sciences of the U.S.A. 89, 9444–9448.CrossRefGoogle Scholar
Di Marco, E., Cutuli, N., Guerra, L., Cancedda, R. & Deluca, M. (1993). Molecular cloning of trk E, a novel trk-related putative tyrosine kinase receptor isolated from normal human keratinicytes and widely expressed by normal human tissues. Journal of Biological Chemistry 268, 24290–24295.CrossRefGoogle Scholar
Dinopoulos, A., Eadie, L.A., Dori, I. & Parnavelas, J.G. (1989). The development of basal forebrain projections to the rat visual cortex. Experimental Brain Research 76, 563–571.CrossRefGoogle Scholar
Domenici, L., Berardi, N., Carmignoto, G., Vantini, G. & Maffei, L. (1991). Nerve growth factor prevents the amblyopic effects of monocular deprivation. Proceedings of the National Academy of Sciences of the U.S.A. 88, 8811–8815.CrossRefGoogle ScholarPubMed
Domenici, L., Cellerino, A. & Maffei, L. (1993). Monocular deprivation effects in the rat visual cortex and lateral geniculate nucleus are prevented by nerve growth factor (NGF). II. Lateral geniculate nucleus. Proceedings of the Royal Society B (London) 251, 25–31.Google ScholarPubMed
Dori, I. & Parnavelas, J.G. (1989). The cholinergic innervation of the rat cerebral cortex shows two distinct phases in development. Experimental Brain Research 76, 417–423.CrossRefGoogle ScholarPubMed
Fagiolini, M., Pizzorusso, T., Berardi, N., Domenici, L. & Maffei, L. (1994). Functional postnatal development of the rat primary visual cortex and role of visual experience: Dark rearing and monocular deprivation. Vision Research 34, 709–720.CrossRefGoogle ScholarPubMed
Gage, F.H., Armstrong, D.M., Williams, L.R. & Varon, S. (1988). Morphological response of axotomized septal neurons to nerve growth factor. Journal of Comparative Neurology 269, 147–155.CrossRefGoogle ScholarPubMed
Gage, F.H., Batchelor, P., Chen, K.S., Chin, D., Higgins, G.A., Koh, S., Deputy, S., Rosenberg, M.B., Fischer, W. & Bjorklund, A. (1989). NGF receptor reexpression and NGF mediated cholinergic neuronal hypertrophy in the damaged adult neostriatum. Neuron 2, 1177–1184.CrossRefGoogle ScholarPubMed
Gnahn, H., Hefti, F., Heumann, R., Schwab, M.E. & Thoenen, H. (1983). NGF-mediated increase of choline acetyltransferase (ChAT) in the neonatal forebrain: Evidence for a physiological role of NGF in the brain? Developmental Brain Research 9, 45–52.CrossRefGoogle Scholar
Hayashi, M., Yamashita, A. & Shimizu, K. (1990). Nerve growth factor in the primate central nervous system: Regional distribution and ontogeny. Neuroscience 36, 683–689.CrossRefGoogle ScholarPubMed
Hefti, F. (1986). Nerve growth factor promotes survival of septal cholinergic neurons after fimbrial transections. Journal of Neuroscience 6, 2155–2162.CrossRefGoogle ScholarPubMed
Henderson, Z. (1981). A projection from acetyl cholinesterase containing neurons in the diagonal band to the occipital cortex of the rat. Neuroscience 6, 1081–1088.CrossRefGoogle Scholar
Johnson, E.M. Jr., Lanahan, A., Buck, C.R., Sehgal, A., Morgan, C., Mercer, E., Bothwell, M. & Chao, M.V. (1986). Expression and structure of the human NGF receptor. Cell 47, 545–554.CrossRefGoogle ScholarPubMed
Kaplan, D.R., Hempstead, B.L., Martin-Zanca, D., Chao, M.V. & Parada, L.F. (1991). The trk protooncogene product: A signal transducing receptor for nerve growth factor. Science 252, 554–558.CrossRefGoogle ScholarPubMed
Knipper, M., Beck, A., Rylett, J. & Breer, H. (1993). Neurotrophin induced 2nd messenger responses in rat brain synaptosomes. Neuro-Report 4(5): 483–486.Google Scholar
Koh, S. & Higgins, G.A. (1991). Differential regulation of the low-affinity nerve growth factor receptor during postnatal development of the rat brain. Journal of Comparative Neurology 313, 494–508.CrossRefGoogle ScholarPubMed
Korshing, S. & Thoenen, H. (1983). Quantitative demonstration of the retrograde axonal transport of endogenous nerve growth factor. Neuroscience Letters 39, 1–4.CrossRefGoogle Scholar
Lapchak, P.A., Araujo, D.M., Carswell, S. & Hefti, F. (1993). Distribution of 125I nerve growth factor in the rat brain following a single intraventricular injection: Correlation with the topographical distribution of trk A messenger expressing cells. Neuroscience 54, 445–460.CrossRefGoogle ScholarPubMed
Large, T.H., Bodary, S.C., Clegg, D.O., Weskamp, G., Otten, U. & Reichardt, L.F. (1986). Nerve growth factor gene expression in the developing rat brain. Science 234, 352–355.CrossRefGoogle ScholarPubMed
Leibrock, J., Lottspeich, F., Hohn, A., Hofer, M., Hengerer, B., Masiakowski, P., Thoenen, H. & Barde, Y.A. (1989). Molecular cloning and expression of brain-derived neurotrophic factor. Nature 341, 149–152.CrossRefGoogle ScholarPubMed
Levi-Montalcini, R. (1987). The nerve growth factor 35 years later. Science 237, 1154–1162.CrossRefGoogle ScholarPubMed
Levi-Montalcini, R. & Angeletti, P.U. (1968). Nerve growth factor. Physiological Reviews 48, 534–569.CrossRefGoogle ScholarPubMed
Lohof, A.M., IP, N.Y. & Poo, M. (1993). Potentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF. Nature 363, 350–353.CrossRefGoogle ScholarPubMed
Maffei, L., Berardi, N., Domenici, L., Parisi, V. & Pizzorusso, T. (1992). Nerve growth factor (NGF) prevents the shift in ocular dominance distribution of visual cortical neurons in monocularly deprived rats. Journal of Neuroscience 12, 4651–4662.CrossRefGoogle ScholarPubMed
Meakin, S.O. & Shooter, E.M. (1991 a). Molecular investigations on the high affinity nerve growth factor-receptor. Neuron 6, 153–163.CrossRefGoogle ScholarPubMed
Meakin, S.O. & Shooter, E.M. (1991 b). Tyrosine kinase activity coupled to the high affinity nerve growth factor-receptor complex. Proceedings of the National Academy of Sciences of the U.S.A. 88, 5862–5866.CrossRefGoogle Scholar
Meakin, S.O. & Shooter, E.M. (1992). The nerve growth factor receptors. Trends in Neuroscience 15, 323–331.CrossRefGoogle Scholar
Milner, T.A., Loy, R. & Amaral, D.G. (1983). An anatomical study of the development of the septo-hippocampal projection in the rat. Developmental Brain Research 8, 343–371.CrossRefGoogle Scholar
Palmetier, M.A., Hartman, B.K. & Johnson, E.M. Jr. (1984). Demonstration of retrogradely transported endogenous nerve growth factor in axons of sympathetic neurons. Journal of Neuroscience 4, 751–756.CrossRefGoogle Scholar
Paxinos, G. & Watson, C. (1982). The Rat Brain in Stereotaxic Coordinates. New York: Academic Press.Google Scholar
Paxinos, G., Tork, I., Tecott, L.H. & Valentino, K.L. (1986). The Atlas of the Developing Rat Brain. San Diego, California: Academic Press.Google Scholar
Peters, A. & Fairen, A. (1978). Smooth and sparsely-spined stellate cells in the visual cortex of the rat: A study using a combined Golgi-electron microscope technique. Journal of Comparative Neurology 181, 129–172.CrossRefGoogle Scholar
Radeke, M.J., Misko, T.P., Hsu, C., Herzemberg, L.A. & Shooter, E.M. (1987). Gene transfer and molecular cloning of the rat nerve growth factor receptor. Nature 325, 593–597.CrossRefGoogle ScholarPubMed
Ringsted, T., Iagercrantz, H. & Persson, H. (1993). Expression of members of the Trk family in the developing postnatal brain. Developmental Brain Research 72, 119–131.CrossRefGoogle Scholar
Rye, D.B., Wainer, B.H., Mesulam, M.M., Mufson, E.J. & Safer, C.B. (1984). Cortical projections arising from the basal forebrain: A study of cholinergic and noncholinergic components employing combined retrograde tracing and immunohistochemical localization of choline acetyltransferase. Neuroscience 13, 627–643.CrossRefGoogle ScholarPubMed
Schambra, U.B., Sulik, K.K., Petrusz, P. & Lauder, J.M. (1989). Ontogeny of cholinergic neurons in the mouse forebrain. Journal of Comparative Neurology 288, 101–122.CrossRefGoogle ScholarPubMed
Semba, K. & Fibinger, H.C. (1988). Time origin of cholinergic neurons in the rat basal forebrain. Journal of Comparative Neurology 269, 87–95.CrossRefGoogle ScholarPubMed
Shatz, C.J. (1990). Impulse activity and the patterning of connections during CNS development. Neuron 5, 745–756.CrossRefGoogle ScholarPubMed
Sieler, M. & Schwab, M.E. (1984). Specific retrograde transport of nerve growth factor (NGF) from neocortex to nucleus basalis in the rat. Brain Research 300, 33–39.CrossRefGoogle Scholar
Stafford, C.A. (1984). Critical period plasticity for visual function: Definition in monocularly deprived rats using visually evoked potentials. Ophthalmic and Physiological Optics 4, 95–100.CrossRefGoogle ScholarPubMed
Stockel, K., Paravicini, V. & Thoenen, H. (1974). Specificity of the retrograde axonal transport of nerve growth factor. Brain Research 76, 413–421.CrossRefGoogle ScholarPubMed
Thoenen, H. & Barde, Y.A. (1980). Physiology of the nerve growth factor. Physiological Reviews 60, 1284–1335.CrossRefGoogle ScholarPubMed
Thoenen, H. (1991). The changing scene of neurotrophic factors. Trends in Neuroscience 14, 165–170.CrossRefGoogle ScholarPubMed
Valenzuela, D.M., Maisonpierre, P.C., Glass, D.J., Rojas, E., Nunez, L., Kong, Y., Gies, D.R., Stitt, T.N., Ip, N.Y. & Yan-Copoulos, G.D. (1993). Alternative forms of rat Trk C with different functional capabilities. Neuron 10, 963–974.CrossRefGoogle Scholar
Widmer, H.R., Kaplan, D.R., Rabin, S.T., Beck, K.D., Hefti, F. & Knusel, B. (1993). Rapid phosphorilation of phospholypase Cγ1 by brain-derived neurotrophic factor and neurotrophin-3 in cultures of embryonic rat cortical neurons. Journal of Neurochemistry 60, 2111–2123.CrossRefGoogle Scholar
Yan, Q. & Johnson, E.M. Jr. (1988). An immunohistochemical study of the nerve growth factor receptor in developing rats. Journal of Neuroscience 8, 3481–3498.CrossRefGoogle ScholarPubMed