Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-24T17:49:28.310Z Has data issue: false hasContentIssue false
  • English
  • Français

Monocular deprivation provokes alteration of the neuronal cytoskeleton in developing cat lateral geniculate nucleus

Published online by Cambridge University Press:  01 May 2009

KEVIN R. DUFFY  and
JOANNA E. SLUSAR
KEVIN R. DUFFY*
Affiliation:
Department of Psychology, Dalhousie University, Life Sciences Centre, Halifax, Nova Scotia, Canada
JOANNA E. SLUSAR
Affiliation:
Department of Psychology, Dalhousie University, Life Sciences Centre, Halifax, Nova Scotia, Canada
*
*Address correspondence and reprint requests to: Kevin R. Duffy, Department of Psychology/Neuroscience, Dalhousie University, 1355 Oxford St., Halifax, Nova Scotia, Canada B3H4J1. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Monocular deprivation early in development produces considerable change in the organization of connections within the central mammalian visual system. In the dorsal lateral geniculate nucleus, the soma, dendrites, and axon terminal fields of deprived cells become considerably smaller than nondeprived counterparts. We have examined the possibility that subcellular events enabling structural modification of deprived neurons include modification of proteins comprising the cytoskeleton. We examined the integrity of the cytoskeleton by measuring the response of a subset of its proteins to varying durations of monocular deprivation. Loss of all three neurofilament subunits (light, medium, and heavy) within deprived layers was observed to parallel changes in neuron gross structure. Monocular deprivation initiated beyond early life produced neither a change in structure nor a loss of neurofilament labeling.

Keywords

Visual SystemStructureNeurofilamentPlasticitydLGNDevelopment
Type
Research Articles
Information
Visual Neuroscience , Volume 26 , Issue 3 , May 2009 , pp. 319 - 328
Copyright
Copyright © Cambridge University Press 2009

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

Antonini, A & Stryker, M.P. (1993). Rapid remodeling of axonal arbors in the visual cortex. Science 260, 1819–1821.CrossRefGoogle ScholarPubMed
Bickford, M.E., Guido, W. & Godwin, D.W. (1998). Neurofilament proteins in Y-cells of the cat lateral geniculate nucleus: Normal expression and alteration with visual deprivation. The Journal of Neuroscience 18, 6549–6557.CrossRefGoogle ScholarPubMed
Blake, R. & Di Gianfilippo, A. (1980). Spatial vision in cats with selective neural deficits. Journal of Neurophysiology 43, 1197–1205.CrossRefGoogle ScholarPubMed
Cleland, B.G., Harding, T.H. & Tulunay-Keesey, U. (1979). Visual resolution and receptive field size: Examination of two kinds of cat retinal ganglion cell. Science 205, 1015–1017.CrossRefGoogle ScholarPubMed
Crozier, R.A., Wang, Y., Liu, C.H. & Bear, M.F. (2007). Deprivation-induced synaptic depression by distinct mechanisms in different layers of mouse visual cortex. Proceedings of the National Academy of Sciences of the United States of America 104, 1383–1388.CrossRefGoogle ScholarPubMed
del Cerro, S., Arai, A., Kessler, M., Bahr, B.A., Vanderklish, P., Rivera, S. & Lynch, G. (1994). Stimulation of NMDA receptors activates calpain in cultured hippocampal slices. Neuroscience Letters 167, 149–152.CrossRefGoogle ScholarPubMed
Duffy, K.R. & Livingstone, M.S. (2005). Loss of neurofilament labeling in the primary visual cortex of monocularly deprived monkeys. Cerebral Cortex 15, 1146–1154.CrossRefGoogle ScholarPubMed
Duffy, K.R., Murphy, K.M., Frosch, M.P. & Livingstone, M.S. (2007). Cytochrome oxidase and neurofilament reactivity in monocularly deprived human primary visual cortex. Cerebral Cortex 17, 1283–1291.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. The Journal of Physiology 187, 517–552.CrossRefGoogle ScholarPubMed
Friedlander, M.J., Stanford, L.R. & Sherman, S.M. (1982). Effects of monocular deprivation on the structure-function relationship of individual neurons in the cat’s lateral geniculate nucleus. The Journal of Neuroscience 2, 321–330.CrossRefGoogle ScholarPubMed
Georges, E. & Mushynski, W.E. (1987). Chemical modification of charged amino acid moieties alters the electrophoretic mobilities of neurofilament subunits on SDS/polyacrylamide gels. European Journal of Biochemistry 165, 281–287.CrossRefGoogle ScholarPubMed
Guillery, R.W. & Stelzner, D.J. (1970). The differential effects of unilateral lid closure upon the monocular and binocular segments of the dorsal lateral geniculate nucleus in the cat. The Journal of Comparative Neurology 139, 413–421.CrossRefGoogle ScholarPubMed
Henry, S.H. & Bhandari, M.A. (1992). Neuronal organization and plasticity in adult monkey visual cortex: Immunoreactivity for microtubule-associated protein 2. Visual Neuroscience 9, 445–459.CrossRefGoogle Scholar
Heynen, A.J., Yoon, B.J., Liu, C.H., Chung, H.J., Huganir, R.L. & Bear, M.F. (2003). Molecular mechanism for loss of visual cortical responsiveness following brief monocular deprivation. Nature Neuroscience 6, 854–862.CrossRefGoogle ScholarPubMed
Hoffman, P.N., Cleveland, D.W., Griffin, J.W., Landes, P.W., Cowan, N.J. & Price, D.L. (1987). Neurofilament gene expression: A major determinant of axonal caliber. Proceedings of the National Academy of Sciences of the United States of America 84, 3472–3476.CrossRefGoogle Scholar
Hoffman, P.N. & Lasek, R.J. (1975). The slow component of axonal transport. The Journal of Cell Biology 66, 351–366.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1970). The period of susceptibility to the physiological effects of unilateral eye closure in kittens. The Journal of Physiology 206, 419–436.CrossRefGoogle Scholar
Johnson, G.V., Litersky, J.M. & Jope, R.S. (1991). Degradation of microtubule-associated protein 2 and brain spectrin by calpain: A comparative study. Journal of Neurochemistry 56, 1630–1638.CrossRefGoogle ScholarPubMed
Julien, J.P. & Mushynski, W.E. (1982). Multiple phosphorylation sites in mammalian neurofilament polypeptides. The Journal of Biological Chemistry 257, 10467–10470.CrossRefGoogle ScholarPubMed
Kamakura, K., Ishiura, S., Suzuki, K., Sugita, H. & Toyokura, Y. (1985). Calcium-activated neutral protease in the peripheral nerve, which requires microM order Ca2+, and its effect on the neurofilament triplet. Journal of Neuroscience Research 13, 391–403.CrossRefGoogle ScholarPubMed
Kaufmann, E., Geisler, N. & Weber, K. (1984). SDS-PAGE strongly overestimates the molecular masses of the neurofilament proteins. FEBS Letters 170, 81–84.CrossRefGoogle ScholarPubMed
Kleinschmidt, A., Bear, M.F. & Singer, W. (1987). Blockage of “NMDA” receptors disrupts experience-dependent plasticity of kitten striate cortex. Science 238, 355–358.CrossRefGoogle Scholar
Kutcher, M.R. & Duffy, K.R. (2007). Cytoskeletal alteration correlates with gross structural plasticity in the cat lateral geniculate nucleus. Visual Neuroscience 24, 775–785.CrossRefGoogle ScholarPubMed
Lomber, S.G., Payne, B.R., Cornwell, P. & Pearson, H.E. (1993). Capacity of the retinogeniculate pathway to reorganize following ablation of visual cortical areas in developing and mature cats. The Journal of Comparative Neurology 338, 432–457.CrossRefGoogle ScholarPubMed
Millecamps, S., Gowing, G., Corti, O., Mallet, J. & Julien, J.P. (2007). Conditional NF-L transgene expression in mice for in vivo analysis of turnover and transport rate of neurofilaments. The Journal of Neuroscience 27, 4947–4956.CrossRefGoogle ScholarPubMed
Mioche, L. & Singer, W. (1989). Chronic recordings from single sites of kitten striate cortex during experience-dependent modification of receptive-field properties. Journal of Neurophysiology 62, 185–197.CrossRefGoogle ScholarPubMed
Morris, J.R. & Lasek, R.J. (1982). Stable polymers of the axonal cytoskeleton: The axoplasmic ghost. The Journal of Cell Biology 92, 192–198.CrossRefGoogle ScholarPubMed
Murphy, K.M. & Mitchell, D.E. (1987). Reduced visual acuity in both eyes of monocularly deprived kittens following a short or long period of reverse occlusion. The Journal of Neuroscience 7, 1526–1536.CrossRefGoogle ScholarPubMed
Nixon, R.A. & Logvinenko, K.B. (1986). Multiple fates of newly synthesized neurofilament proteins: Evidence for a stationary neurofilament network distributed nonuniformly along axons of retinal ganglion cell neurons. The Journal of Cell Biology 102, 647–659.CrossRefGoogle ScholarPubMed
Olson, C.R. & Freeman, R.D. (1980). Profile of the sensitive period for monocular deprivation in kittens. Experimental Brain Research 39, 17–21.CrossRefGoogle ScholarPubMed
Sanderson, K.J. (1971). The projection of the visual field to the lateral geniculate and medial interlaminar nuclei in the cat. The Journal of Comparative Neurology 143, 101–118.CrossRefGoogle Scholar
Sato, M. & Stryker, M.P. (2008). Distinctive features of adult ocular dominance plasticity. The Journal of Neuroscience 28, 10278–10286.CrossRefGoogle ScholarPubMed
Schlaepfer, W.W. & Zimmerman, U.J. (1985). Calcium-activated proteolysis of intermediate filaments. Annals of New York Academy of Sciences 455, 552–562.CrossRefGoogle ScholarPubMed
Sherman, S.M., Hoffmann, K.P. & Stone, J. (1972). Loss of specific cell type from dorsal lateral geniculate nucleus in visually deprived cats. Journal of Neurophysiology 35, 532–541.CrossRefGoogle ScholarPubMed
Stone, J. (1973). Sampling properties of microelectrodes assessed in the cat’s retina. Journal of Neurophysiology 36, 1071–1079.CrossRefGoogle ScholarPubMed
Sur, M., Humphrey, A.L. & Sherman, S.M. (1982). Monocular deprivation affects X- and Y-cell retinogeniculate terminations in cats. Nature 300, 183–185.CrossRefGoogle ScholarPubMed
Van der Gucht, E., Vandesande, F. & Arckens, L. (2001). Neurofilament protein: A selective marker for the architectonic parcellation of the visual cortex in adult cat brain. The Journal of Comparative Neurology 441, 345–368.CrossRefGoogle ScholarPubMed
Wiesel, T.N. & Hubel, D.H. (1963 a). Single-cell responses in striate cortex of kittens deprived of vision in one eye. Journal of Neurophysiology 26, 1003–1017.CrossRefGoogle ScholarPubMed
Wiesel, T.N. & Hubel, D.H. (1963 b). Effects of visual deprivation on morphology and physiology of cells in the cats lateral geniculate body. Journal of Neurophysiology 26, 978–993.CrossRefGoogle ScholarPubMed