Hostname: page-component-8448b6f56d-mp689 Total loading time: 0 Render date: 2024-04-24T07:51:18.370Z Has data issue: false hasContentIssue false
  • English
  • Français

Postnatal development of functional properties of visual cortical cells in rats with excitotoxic lesions of basal forebrain cholinergic neurons

Published online by Cambridge University Press:  02 June 2009

Rosita Siciliano ,
Gigliola Fontanesi ,
Fiorella Casamenti ,
Nicoletta Berardi ,
Paola Bagnoli  and
Luciano Domenici
Rosita Siciliano
Affiliation:
Department of Physiology and Biochemistry, University of Pisa, 56123 Pisa, Italy
Gigliola Fontanesi
Affiliation:
Department of Physiology and Biochemistry, University of Pisa, 56123 Pisa, Italy
Fiorella Casamenti
Affiliation:
Department of Pharmacology, University of Florence, 50134 Florence, Italy
Nicoletta Berardi
Affiliation:
Department of General Psychology, University of Florence, 50134 Florence, Italy
Paola Bagnoli
Affiliation:
Department of Physiology and Biochemistry, University of Pisa, 56123 Pisa, Italy
Luciano Domenici
Affiliation:
Institute of Neurophysiology, Italian Research Council, 56123 Pisa, Italy
Get access Rights & Permissions [Opens in a new window]

Abstract

In the rat, visual cortical cells develop their functional properties during a period termed as critical period, which is included between eye opening, i.e.˘postnatal day (PD) 15, and PD40. The present investigation was aimed at studying the influence of cortical cholinergic afferents from the basal forebrain (BF) on the development of functional properties of visual cortical neurons. At PD15, rats were unilaterally deprived of the cholinergic input to the visual cortex by stereotaxic injections of quisqualic acid in BF cholinergic nuclei projecting to the visual cortex. Cortical cell functional properties, such as ocular dominance, orientation selectivity, receptive-field size, and cell responsiveness were then assessed by extracellular recordings in the visual cortex ipsilateral to the lesioned BF both during the critical period (PD30) and after its end (PD45). After the recording session, the rats were sacrificed and the extent of both cholinergic lesion in BF and cholinergic depletion in the visual cortex was determined. Our results show that lesion of BF cholinergic nuclei transiently alters the ocular dominance of visual cortical cells while it does not affect the other functional properties tested. In particular, in lesioned animals recorded during the critical period, a higher percentage of visual cortical cells was driven by the contralateral eye with respect to normal animals. After the end of the critical period, the ocular dominance distribution of animals with cholinergic deafferentation was not significantly different from that of controls. Our results suggest the possibility that lesions of BF cholinergic neurons performed during postnatal development only transiently interfere with cortical competitive processes.

Keywords

Postnatal developmentOcular dominanceOrientation sensitivityReceptive-field sizeAcetylcholineVisual cortexRat
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 1 , January 1997 , pp. 111 - 123
Copyright
Copyright © Cambridge University Press 1997

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.)

References

Albus, K. & Wolf, W. (1984). Early post-natal development of neuronal function in the kitten's visual cortex: A laminar analysis. Journal of Physiology (London) 348, 153–185.CrossRefGoogle ScholarPubMed
Batchelor, P.E., Armstrong, D.M., Blaker, S.N. & Gage, F.H. (1989). Nerve growth factor receptor and choline acetyltransferase colocalization in neurons within the rat forebrain: Response to fimbria-fornix transection. Journal of Comparative Neurology 284, 187–204.CrossRefGoogle ScholarPubMed
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., Pizzorusso, 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., Cellerino, A., Domenici, L., Fagiolini, M., Pizzorusso, T., Cattaneo, A. & Maffei, L. (1994). Monoclonal antibodies to nerve growth factor affect the postnatal development of the visual system. Proceedings of the National Academy of Sciences of the U.S.A. 91, 684–688.CrossRefGoogle ScholarPubMed
Blakemore, C. & Van Sluyters, R.C. (1975). Innate and environmental factors in the development of the kitten's visual cortex. Journal of Physiology (London) 248, 663–716.CrossRefGoogle ScholarPubMed
Boothe, R.G., Dobson, V. & Teller, D.Y. (1985). Postnatal development of vision in human and in non human primates. Annual Review of Neuroscience 8, 495–545.CrossRefGoogle Scholar
Bradford, M.M. (1976). A rapid sensitive method for quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254CrossRefGoogle Scholar
Chandler, C.E., Parsons, L.M., Hosang, M. & Shooter, E.M. (1984). A monoclonal antibody modulates the interaction of nerve growth factor with PC 12 cells. Journal of Biological Chemistry 259, 6882–6889.CrossRefGoogle Scholar
Dawbarn, D., Allen, S.J. & Semenenko, P.M. (1988). Coexistence of choline acetyltransferase and nerve growth factor receptors in the rat basal forebrain. Neuroscience Letters 94, 138–164.CrossRefGoogle ScholarPubMed
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, C., 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
Domenici, L., Cellerino, A., Berardi, N., Cattaneo, A. & Maffei, L. (1994). Antibodies to nerve growth factor (NGF) prolong the sensitive period for monocular deprivation in the rat. Neuroreport 5, 2041–2044.CrossRefGoogle ScholarPubMed
Dunnett, S.B., Whishaw, I.Q., Jones, G.H. & Bunch, S.T. (1987). Behavioural, biochemical and histochemical effects of different neurotoxic amino acids injected into nucleus basalis magnocellularis of rats. Neuroscience 20, 653–669.CrossRefGoogle ScholarPubMed
Dunnett, S.B., Everitt, B.J. & Robbins, T.W. (1991). The basal forebrain cortical cholinergic system: Interpreting the functional consequences of excitotoxic lesions. Trends in Neuroscience 14, 494–501.CrossRefGoogle ScholarPubMed
Eckenstein, P.P., Baughman, R.W. & Quinn, J. (1988). An anatomical study of cholinergic innervation in rat cerebral cortex. Neuroscience 25, 457–474.CrossRefGoogle ScholarPubMed
Fagiolini, M., Pizzorusso, T., Berardi, N., Domenici, L. & Maffei, L. (1994). Functional postnatal development of the rat primary visual cortex and the role of visual experience: Dark rearing and monocular deprivation. Vision Research 34, 709–720.CrossRefGoogle ScholarPubMed
Fine, A., Dunnett, S.B., Björklund, A., Clark, D. & Iversen, S.D. (1985). Transplantation of embryonic ventral forebrain neurons to the neocortex of rats with lesions of nucleus basalis magnocellularis. I. Biochemical and anatomical observations. Neuroscience 16, 769–786.CrossRefGoogle Scholar
Fonnum, F.A. (1975). A rapid radiochemical method for the determination of choline acetyltransferase. Journal of Neurochemistry 24, 407–409.CrossRefGoogle ScholarPubMed
Fox, K. & Zahs, K. (1994). Critical period control in sensory cortex. Current Opinion Neurobiology 4, 112–119.CrossRefGoogle ScholarPubMed
Fuxe, K., Hamberger, B. & Hökfelt, T. (1968). Distribution of noradrenaline nerve terminals in cortical areas of the rat. Brain Research 8, 125–131.CrossRefGoogle ScholarPubMed
Gnahn, H., Hefti, F., Heumann, R., Schwab, M.E. & Thoenen, H. (1983). NGF-mediated increase in choline acetyltransferase (ChAT) in the neonatal rat forebrain: Evidence for a physiological role of NGF in the brain? Development Brain Research 9, 45–52.CrossRefGoogle Scholar
Gu, Q. & Singer, W. (1993). Effects of intracortical infusion of anticholinergic drugs on neuronal plasticity in kitten striate cortex. European Journal of Neuroscience 5, 475–485.CrossRefGoogle ScholarPubMed
Halliwell, J.V. & Adams, P.R. (1982). Voltage-clamp analysis of muscarinic excitation in hippocampal neurons. Brain Research 250, 71–92.CrossRefGoogle ScholarPubMed
Hancock, M.B. (1984). Visualization of peptide-immunoreactive processes of serotonin immunoreactive cells using two color immunoperoxidase staining. Journal ofHistochemistry and Cytochemistry 37, 311–314.CrossRefGoogle Scholar
Hebb, D.O. (1949). Organization of Behavior. New York: John Wiley and Sons.Google Scholar
Higgins, G.A., Koh, S., Chen, K.S. & Gage, F.H. (1989). NGF induction of NGF receptor gene expression and cholinergic neuronal hypertrophy within the basal forebrain of the adult rat. Neuron 3, 247–256.CrossRefGoogle ScholarPubMed
Houser, C.R., Crawford, G.D., Salvaterra, P.M. & Vaughn, J.E. (1985). Immunocytochemical localization of choline acetyltransferase in rat cerebral cortex: A study of cholinergic neurons and synapses. Journal of Comparative Neurology 234, 17–34.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. Journal of Physiology 160, 106–154.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1963). Receptive fields of cells in striate cortex of very young, visually inexperienced kitten. Journal of Neuro-physiology 26, 994–1002.CrossRefGoogle Scholar
Hughes, A. (1979). A schematic eye for the rat. Vision Research 19, 569–588.CrossRefGoogle ScholarPubMed
Juliano, S.E., Ma, W. & Eslin, D. (1991). Cholinergic depletion prevents expansion of topographic maps in somatosensory cortex. Proceedings of the National Academy of Sciences of the U.S.A. 88, 780–784.CrossRefGoogle ScholarPubMed
Kasamatsu, T. & Pettigrew, J.D. (1979). Preservation of binocularity after monocular deprivation in the striate cortex of kittens treated with 6-hydroxydopamine. Journal of Comparative Neurology 185, 139–161.CrossRefGoogle ScholarPubMed
Kasamatsu, T. & Heggelund, P. (1982). Single cell responses in the cat visual cortex to visual stimulation during iontophoresis of noradrenaline. Experimental Brain Research 45, 317–327.CrossRefGoogle ScholarPubMed
Kiss, J., McGovern, J. & Patel, A.J. (1988). Immunohistochemical localization of cells containing nerve growth factor receptors in the different regions of the adult rat forebrain. Neuroscience 27, 731–748.CrossRefGoogle ScholarPubMed
Levitt, P. & Moore, R.Y. (1978). Noradrenaline neuron innervation of the neocortex in the rat. Brain Research 139, 219–231.CrossRefGoogle ScholarPubMed
Madison, D.V. & Nicoll, R.A. (1982). Noradrenaline blocks accommodation of pyramidal cell discharge in the hippocampus. Nature 299, 636–638.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
Mesulam, M.M., Mufson, E.J., Wainer, B.H. & Levey, A.I. (1983). Central cholinergic pathway in the rat: An overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10, 1185–1201.CrossRefGoogle Scholar
Parnavelas, J.G., Burne, R.A. & Lin, C.S. (1981). Receptive field properties of neurons in the visual cortex of the rat. Neuroscience Letters 27, 291–296.CrossRefGoogle ScholarPubMed
Parnavelas, J.G., Kelly, W., Franke, E. & Eckenstein, F. (1986). Cholinergic neurons and fibres in the rat visual cortex. Journal of Neurocytology 15, 329–336.CrossRefGoogle ScholarPubMed
Paxinos, G. & Watson, C. (1986). The Rat Brain in Stereotaxic Coordinates. Sydney, Australia: Academic Press.Google Scholar
Pickel, V.M., Segal, M. & Bloom, F.E. (1974). A radioautographic study of the efferent pathways of the nucleus locus coeruleus. Journal of Comparative Neurology 155, 15–42.CrossRefGoogle ScholarPubMed
Reese, B.E. (1988). “Hidden lamination” in the dorsal lateral geniculate nucleus: The functional organization of this talamic region in the rat. Brain Research Reviews 13, 119–137.CrossRefGoogle Scholar
Saper, C.B. (1984). Organization of cerebral cortical afferent systems in the rat. II. Magnocellular basal nucleus. Journal of Comparative Neurology 222, 313–342.CrossRefGoogle ScholarPubMed
Sato, H., Hata, Y., Masui, H. & Tsumoto, T. (1987). A functional role of cholinergic innervation to neurons in the cat visual cortex. Journal of Neurophysiology 58, 765–780.CrossRefGoogle ScholarPubMed
Seiler, M. & Schwab, M. (1984). Specific retrograde transport of nerve growth factor (NGF) from neocortex to nucleus basalis in the rat. Brain Research 300, 33–39.CrossRefGoogle ScholarPubMed
Shatz, C.J. (1990). Impulse activity and the patterning of connections during CNS development. Neuron 5, 745–756.CrossRefGoogle ScholarPubMed
Shaw, C. & Cynader, M. (1984). Disruption of cortical activity prevents ocular dominance changes in monocularly deprived kittens. Nature 308, 731–734.CrossRefGoogle ScholarPubMed
Sillito, A.M. & Kemp, J.A. (1983). Cholinergic modulation of the functional organization of the cat visual cortex. Brain Research 289, 143–155.CrossRefGoogle ScholarPubMed
Sofroniew, M.V., Cooper, J.D., Svendsen, C.N., Grossman, P., Ip, N.Y., Lindsay, R.M., Zafra, F. & Lindholm, D. (1993). Atrophy but not death of adult septal cholinergic neurons after ablation of target capacity to produce mRNAs for NGF, BDNF, and NT3. Journal of Neuroscience 12, 5263–5276.CrossRefGoogle Scholar
Taniuchi, M., Schweitzer, J.B. & Johnson, E.M.J. (1986). Nerve growth factor receptor molecules in rat brain. Proceedings of the National Academy of Sciences of the U.S.A. 83, 1950–1954.CrossRefGoogle ScholarPubMed
Thoenen, H. (1995). Neurotrophins and neuronal plasticity. Science 270, 593–598.CrossRefGoogle ScholarPubMed
Timney, B. (1987). Dark rearing and the sensitive period for monocular deprivation. In Imprinting and Cortical Plasticity, ed. Rauschecker, J.P. & Marler, P., pp. 95–118. New York: John Wiley and Sons.Google Scholar
Walsh, T.J., Herzog, C., Gandhi, C., Stakman, R.W. & Wiley, R.G. (1995). Intraseptal 192-saporin produces dose and delay-dependent working memory deficits and cholinergic hypofunction. Society for Neuroscience Abstracts 21, 167.Google Scholar
Woolf, N.J., Gould, E. & Butcher, L.L. (1989). Nerve growth factor receptor is associated with cholinergic neurons of the basal forebrain but not the pontomesencephalon. Neuroscience 30, 143–152.CrossRefGoogle Scholar